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Revisiting the microsurgical anatomy of the sagittal stratum and surgical implications: fiber microdissection and tractography study

Beste Gülsuna, Abuzer Güngör, Pınar Yazgan, Gökberk Erol, Erik H. Middlebrooks, Alp Özgün Börcek, Wolfgang J. Weninger, and Uğur Türe

OBJECTIVE

The term "sagittal stratum" was coined by Heinrich Sachs in 1892 to define a parasagittally oriented white matter layer at the temporo-occipital cortex. Although this term has been widely used for more than 100 years, the description, classification, borders, and involved fibers of the structure vary among authors and remain imprecise. Through fiber microdissection and tractography, the authors aimed to define the sagittal stratum and resolve the uncertainty by revealing the relationship of this structure to other cerebral white matter pathways and the orientation of fibers in it.

METHODS

Twenty postmortem human cerebral hemispheres were prepared according to Klingler’s method. Fiber dissections were performed under a surgical microscope and with microsurgical techniques. The results of dissection at each step were photographed with 2D and 3D imaging techniques, and 3D photogrammetry techniques were used to create a 360° model. Diffusion tensor imaging and 7T high-resolution MRI were used to confirm the findings.

RESULTS

This study revisited the 3D organization of white matter tracts in the sagittal stratum through fiber microdissection and tractography. The microneuroanatomical structure of the sagittal stratum and its special organization with fibers from all three fiber systems are demonstrated. The authors’ findings revealed that the sagittal stratum has two layers consisting of four different fiber tracts. Its external layer consists of a long association fiber and a commissural fiber, while its internal layer consists of intertwined projection fibers, including temporo-parieto-occipitopontine fibers and the posterior thalamic peduncle. Detailed microdissection also showed the location of the posterior thalamic peduncle in the most medial site of all posterior hemispheric projection fibers.

CONCLUSIONS

The structure of the sagittal stratum is distinctive in that it contains all three main fiber systems: association, commissural, and projection. Because of its expansive location in the temporal and occipital lobes, it can be damaged by most neurosurgical pathologies and procedures. The authors emphasize the significance of preserving the sagittal stratum during surgical interventions while also challenging the notion of a "silent" brain, suggesting that the current inability to fully comprehend cerebral function contributes to this misconception. Detailed knowledge of the complex white matter anatomy of the sagittal stratum can guide neurosurgeons in surgical planning and the selection of appropriate surgical approaches with intraoperative orientation for safe surgery and less comorbidity.

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Microsurgical anatomy of the olfactory filaments in the nasal mucosa

Hasan Barış Ilgaz, Kamran Urgun, Ulaş Yener, Melike Mut, James K. Liu, and Kaan Yağmurlu

OBJECTIVE

The aim of this study was to examine the distribution of olfactory filaments (OFs) in the nasal mucosa to facilitate preservation of olfactory function in endonasal approaches and preparation of a nasoseptal flap.

METHODS

One formalin-fixed and 9 fresh cadaveric silicone-injected specimens with 20 total sides were studied to measure the distance of the OFs to the anatomical landmarks and compare the OF presence in the nasal septum mucosa (NSM) and ethmoidal mucosa (EM).

RESULTS

The mean distance from the first to the last OF was 19.37 ± 2.16 mm in the NSM and 23.44 ± 5.42 mm in the EM. The NSM had a mean of 7.55 ± 1.31 OFs and the EM had 14.3 ± 1.78. Average OF lengths were measured at 6.44 ± 1.48 (range 3.75–12.40) mm in the NSM and 8.05 ± 1.76 (range 4.14–13.20) mm in the EM. The mean values of the EM measurements were compared with those of the NSM; the number of OFs, the distance between the first and last OF, the average OF length, and the number of OFs between anterior and posterior ethmoidal arteries in the NSM were significantly less (p < 0.05) than those in the EM. The distance between the first OF to the nasal bone on the NSM was greater than on the EM.

CONCLUSIONS

Compared with the EM, the OFs are significantly fewer in number and smaller in size in the NSM. The uppermost edge of the nasoseptal flap incision in the NSM might be safer to start below 12 mm from the cribriform plate for OF protection.

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Ventral amygdalofugal pathway as an integrated surgically important network: microsurgical anatomy and segmentation based on fiber dissection

Buruç Erkan, Batu Hergünsel, Ozan Barut, Tahsin Saygı, Burak Kocak, Abuzer Güngör, Kaan Yağmurlu, and Necmettin Tanriover

OBJECTIVE

The ventral amygdalofugal pathway (VAFP) provides afferent and efferent connections to the amygdala and spans along some of the frequently traversed intra-axial surgical corridors as a dominant fiber bundle. This study aimed to reveal the frequently overlooked VAFP fibers by examining their courses and connections to the basal forebrain, septal region, hypothalamus, thalamus, tegmentum, and brainstem.

METHODS

Ten postmortem human brains were used to display the characteristics of the VAFP, and fiber dissection results were compared with those of tractography.

RESULTS

From anterior to posterior, the VAFP was separated into 5 different portions: 1) amygdala–substantia innominata; 2) amygdaloseptal (diagonal band of Broca); 3) amygdalo-thalamic; 4) amygdalo-hypothalamic, intermingling with the medial forebrain bundle and extending to the bed nucleus of stria terminalis; and 5) amygdalotegmental. The results of fiber dissections were confirmed with findings obtained from diffusion tensor tractography.

CONCLUSIONS

This study supports the concept that interconnected forebrain, diencephalic, mesencephalic, and brainstem connections of the VAFP form an integrated surgically important network. The fiber dissection findings also provide the neuroanatomical basis for VAFP segmentation, which may help neurosurgeons better appreciate the complex microsurgical anatomy of the amygdalar connections. Amygdala–substantia innominata and amygdalotegmental connections are demonstrated for the first time and clarified within the structure of the VAFP.

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Neglected tracts of the brainstem: transverse peduncular tract of Gudden and taenia pontis

Serdar Rahmanov, Abuzer Güngör, Beste Gulsuna, Alberth Patricio Munoz-Gualan, and Uğur Türe

OBJECTIVE

The anatomy and function of the brainstem have fascinated scientists for centuries; however, the brainstem remains one of the least studied regions of the human brain. As the authors delved into studying this structure, they observed a growing tendency to forget or neglect previously identified structures. The aim of this study was to describe two such structures: the transverse peduncular tract, also known as the Gudden tract, and the taenia pontis. The authors analyzed the potential effects of neglecting these structures during brainstem surgery and the implications for clinical practice.

METHODS

After removal of the arachnoid and vascular structures, 20 human brainstem specimens were frozen and stored at −16°C for 2 weeks, according to the method described by Klingler. The specimens were then thawed and dissected with microsurgical techniques. The results of microsurgical fiber dissection at each step were photographed.

RESULTS

This study revealed two previously neglected or forgotten structures within the brainstem. The first is the transverse peduncular tract of Gudden, which arises from the brachium of the superior colliculus. This tract follows an arcuate course along the lateral and ventral surfaces of the midbrain, perpendicular to the cerebral peduncle, and terminates in the nuclei of the transverse peduncular tract within the interpeduncular fossa. The second structure is the taenia pontis, which originates contralaterally in the interpeduncular fossa. It becomes visible at the level of the pontomesencephalic sulcus and extends to the base of the lateral mesencephalic sulcus, where it divides into several thin bundles. Along the interpeduncular sulcus, between the superior and middle cerebellar peduncles, it reaches the parabrachial recess and enters the cerebellum.

CONCLUSIONS

Recently, with increasing understanding and expertise in brainstem research, surgical approaches to this area have become more common, emphasizing the importance of a detailed knowledge of the brainstem. The two structures mentioned in this paper are described in history books and were widely studied in the 19th century but have not been mentioned in modern literature. The authors propose that a deeper understanding of these structures may prove valuable in neurosurgical practice and help reduce patient comorbidity.

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Resection of the quadrangular lobule of the cerebellum to increase exposure of the cerebellomesencephalic fissure: an anatomical study with clinical correlation

Juan Leonardo Serrato-Avila, Juan Alberto Paz Archila, Alejandro Monroy-Sosa, Sebastian Aníbal Alejandro, Marcos Devanir Silva da Costa, Sergio Cavalheiro, Kaan Yagmurlu, Michael T. Lawton, and Feres Chaddad-Neto

OBJECTIVE

The lateral aspect of the cerebellomesencephalic fissure frequently harbors vascular pathology and is a common surgical corridor used to access the pons tegmentum, as well as the cerebellum and its superior and middle peduncles. The quadrangular lobule of the cerebellum (QLC) represents an obstacle to reach these structures. The authors sought to analyze and compare exposure of the cerebellar interpeduncular region (CIPR) before and after QLC resection and provide a case series to evaluate its clinical applicability.

METHODS

Forty-two sides of human brainstems were prepared with Klingler’s method and dissected. The exposure area before and after resection of the QLC was measured and statistically studied. A case series of 59 patients who underwent QLC resection for the treatment of CIPR lesions was presented and clinical outcomes were evaluated at 1-year follow-up.

RESULTS

The anteroposterior surgical corridor of the CIPR increased by 10.3 mm after resection of the QLC. The mean exposure areas were 42 mm2 before resection of the QLC and 159.6 mm2 after resection. In this series, ataxia, extrapyramidal syndrome, and akinetic mutism were found after surgery. However, all these cases resolved within 1 year of follow-up. Modified Rankin Scale score improved by 1 grade, on average.

CONCLUSIONS

QLC resection significantly increased the exposure area, mainly in the anteroposterior axis. This surgical strategy appears to be safe and may help the neurosurgeon when operating on the lateral aspect of the cerebellomesencephalic fissure.

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A new classification of parasagittal bridging veins based on their configurations and drainage routes pertinent to interhemispheric approaches: a surgical anatomical study

Derya Karatas, Jaime L. Martínez Santos, Saygı Uygur, Ahmet Dagtekin, Zeliha Kurtoglu Olgunus, Emel Avci, and Mustafa K. Baskaya

OBJECTIVE

Opening the roof of the interhemispheric microsurgical corridor to access various neurooncological or neurovascular lesions can be demanding because of the multiple bridging veins that drain into the sinus with their highly variable, location-specific anatomy. The objective of this study was to propose a new classification system for these parasagittal bridging veins, which are herein described as being arranged in 3 configurations with 4 drainage routes.

METHODS

Twenty adult cadaveric heads (40 hemispheres) were examined. From this examination, the authors describe 3 types of configurations of the parasagittal bridging veins relative to specific anatomical landmarks (coronal suture, postcentral sulcus) and their drainage routes into the superior sagittal sinus, convexity dura, lacunae, and falx. They also quantify the relative incidence and extension of these anatomical variations and provide several preoperative, postoperative, and microneurosurgical clinical case study examples.

RESULTS

The authors describe 3 anatomical configurations for venous drainage, which improves on the 2 types that have been previously described. In type 1, a single vein joins; in type 2, 2 or more contiguous veins join; and in type 3, a venous complex joins at the same point. Anterior to the coronal suture, the most common configuration was type 1 dural drainage, occurring in 57% of hemispheres. Between the coronal suture and the postcentral sulcus, most veins (including 73% of superior anastomotic veins of Trolard) drain first into a venous lacuna, which are larger and more numerous in this region. Posterior to the postcentral sulcus, the most common drainage route was through the falx.

CONCLUSIONS

The authors propose a systematic classification for the parasagittal venous network. Using anatomical landmarks, they define 3 venous configurations and 4 drainage routes. Analysis of these configurations with respect to surgical routes indicates 2 highly risky interhemispheric surgical fissure routes. The risks are attributable to the presence of large lacunae that receive multiple veins (type 2) or venous complex (type 3) configurations that negatively impact a surgeon’s working space and degree of movement and thus are predisposed to inadvertent avulsions, bleeding, and venous thrombosis.

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Microsurgical and fiber tract anatomy of the interthalamic adhesion

Mehmet Hakan Şahin, Abuzer Güngör, Oğuz Kağan Demirtaş, Çağrı Postuk, Zeynep Fırat, Gazanfer Ekinci, Hakan Hadi Kadıoğlu, and Uğur Türe

OBJECTIVE

The authors of this study aimed to define the microanatomy of the interthalamic adhesion (ITA) using microfiber dissection, magnetic resonance (MR) tractography, and histological analysis.

METHODS

Sagittal, coronal, and axial MR images from 160 healthy individuals 2–82 years of age were examined. The relationships between age range and ITA morphology as well as between gender and ITA morphology were evaluated statistically. Among these 160 individuals, 100 who had undergone MR tractography were examined. In this group, the presence of fiber tracts in the ITA and the relationship with ITA morphological types were examined. Thirty formalin-fixed human cadaveric brains were also examined endoscopically, and 6 hemispheres were dissected from the medial to lateral and superior to inferior directions under the microscope. Sections taken from one of the brains with an ITA type 2 with both thalami were examined histologically. Anti-neurofilament antibody was used in the histological examination.

RESULTS

Four morphological types of ITA were observed. Type 1 had an adhesion/adherent appearance, type 2 had a bridge/commissure appearance, type 3 showed no adhesion, and type 4 had a double bridge. Tractographic examination revealed that 28% had no fiber tract transition in the ITA, 21% had a significant transition, and 51% had an indistinct transition. Statistically, the presence of the ITA was significantly higher in the pediatric (age) and female (gender) groups. In specimens with ITAs of a bridge/commissure appearance (type 2), fiber tracts showed clear transitions between thalami. In type 1 (adherent/adhesive appearance), fiber tracts were observed within the ITA, but a reciprocal transition was unclear. Dissection showed that these fiber tracts in the ITA reach the nucleus accumbens, caudate nucleus, and frontoorbital region anteriorly and the lateral habenula and posterior commissure posteriorly. Some fibers also joined the ansa peduncularis. In histological studies, axonal fibers moving in the ITA were observed with anti-neurofilament antibody staining.

CONCLUSIONS

This is the first study to demonstrate fiber tracts of the ITA through fiber dissection and transillumination techniques as well as radiological and histological study. Statistical data were obtained by comparing the morphological group with age and gender groups. The anatomy of this structure, which has been neglected for many years, was reexamined. This study showed that the ITA has fibers connecting different parts of the brain, in contrast to previous studies suggesting that it was a simple massa.

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Reappraisal of the anatomy of the frontotemporal branches of the facial nerve

Maximiliano Alberto Nunez, Ahmed Mohyeldin, Dario A. Marotta, Vera Vigo, Karam Asmaro, Yuanzhi Xu, Aaron A. Cohen-Gadol, and Juan C. Fernandez-Miranda

OBJECTIVE

The anatomy of the temporal branches of the facial nerve (FN) has been widely described in the neurosurgical literature because of its relevance in anterolateral approaches to the skull base and implication in frontalis palsies from these approaches. In this study, the authors attempted to describe the anatomy of the temporal branches of the FN and identify whether there are any FN branches that cross the interfascial space of the superficial and deep leaflets of the temporalis fascia.

METHODS

The surgical anatomy of the temporal branches of the FN was studied bilaterally in 5 embalmed heads (n = 10 extracranial FNs). Exquisite dissections were performed to preserve the relationships of the branches of the FN and their relationship to the surrounding fascia of the temporalis muscle, the interfascial fat pad, the surrounding nerve branches, and their final terminal endpoints near the frontalis and temporalis muscles. The authors correlated their findings intraoperatively with 6 consecutive patients with interfascial dissection in which neuromonitoring was performed to stimulate the FN and associated twigs that were observed to be interfascial in 2 of them.

RESULTS

The temporal branches of the FN stay predominantly superficial to the superficial leaflet of the temporal fascia in the loose areolar tissue near the superficial fat pad. As they course over the frontotemporal region, they give off a twig that anastomoses with the zygomaticotemporal branch of the trigeminal nerve, which crosses the superficial layer of the temporalis muscle, spanning the interfascial fat pad, and then pierces the deep temporalis fascial layer. This anatomy was observed in 10 of the 10 FNs dissected. Intraoperatively, stimulation of this interfascial segment yielded no facial muscle response up to 1 mA in any of the patients.

CONCLUSIONS

The temporal branch of the FN gives off a twig that anastomoses with the zygomaticotemporal nerve, which crosses the superficial and deep leaflets of the temporal fascia. Interfascial surgical techniques aimed at protecting the frontalis branch of the FN are safe in their efforts to protect against frontalis palsy with no clinical sequelae when executed properly.

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Microsurgical anatomy and insular connectivity of the cerebral opercula

Oğuz Kağan Demirtaş, Abuzer Güngör, Pınar Çeltikçi, Emrah Çeltikçi, Alberth Patricio Munoz-Gualan, Fikret Hüseyin Doğulu, and Uğur Türe

OBJECTIVE

Radiological, anatomical, and electrophysiological studies have shown the insula and cerebral opercula to have extremely high functionality. Because of this complexity, interventions in this region cause higher morbidity compared to those in other areas of the brain. In most early studies of the insula and white matter pathways, insular dissection was begun after the opercula were removed. In this study, the authors examined the insula and deep white matter pathways to evaluate the insula as a whole with the surrounding opercula.

METHODS

Twenty formalin-fixed adult cerebral hemispheres were studied using fiber microdissection techniques and examination of sectional anatomy. Dissections were performed from lateral to medial, medial to lateral, inferior to superior, and superior to inferior. A silicone brain model was used to show the normal gyral anatomy. Sections and fibers found at every stage of dissection were photographed with a professional camera. MRI tractography studies were used to aid understanding of the dissections.

RESULTS

The relationships between the insula and cerebral opercula were investigated in detail through multiple dissections and sections. The relationship of the extreme and external capsules with the surrounding opercula and the fronto-occipital fasciculus with the fronto-orbital operculum was demonstrated. These findings were correlated with the tractography studies. Fibers of the extreme capsule connect the medial aspect of the opercula with the insula through the peri-insular sulcus. Medial to lateral dissections were followed with the removal of the central core structures, and in the last step, the medial surface of the cerebral opercula was evaluated in detail.

CONCLUSIONS

This anatomical study clarifies our understanding of the insula and cerebral opercula, which have complex anatomical and functional networks. This study also brings a new perspective to the connection of the insula and cerebral opercula via the extreme and external capsules.

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Microsurgical anatomy and the importance of the petrosal process of the sphenoid bone in endonasal surgery

Ayoze Doniz-Gonzalez, Vera Vigo, Maximiliano Alberto Nunez, Yuanzhi Xu, Ahmed Mohyeldin, Aaron A. Cohen-Gadol, and Juan C. Fernandez-Miranda

OBJECTIVE

The petrosal process of the sphenoid bone (PPsb) is a relevant skull base osseous prominence present bilaterally that can be used as a key surgical landmark, especially for identifying the abducens nerve. The authors investigated the surgical anatomy of the PPsb, its relationship with adjacent neurovascular structures, and its practical application in endoscopic endonasal surgery.

METHODS

Twenty-one dried skulls were used to analyze the osseous anatomy of the PPsb. A total of 16 fixed silicone-injected postmortem heads were used to expose the PPsb through both endonasal and transcranial approaches. Dimensions and distances of the PPsb from the foramen lacerum (inferiorly) and top of the posterior clinoid process (PCP; superiorly) were measured. Moreover, anatomical variations and the relationship of the PPsb with the surrounding crucial structures were recorded. Three representative cases were selected to illustrate the clinical applications of the findings.

RESULTS

The PPsb presented as a triangular bony prominence, with its base medially adjacent to the dorsum sellae and its apex pointing posterolaterally toward the petrous apex. The mean width of the PPsb was 3.5 ± 1 mm, and the mean distances from the PPsb to the foramen lacerum and the PCP were 5 ± 1 and 11 ± 2.5 mm, respectively. The PPsb is anterior to the petroclival venous confluence, superomedial to the inferior petrosal sinus, and inferomedial to the superior petrosal sinus; constitutes the inferomedial limit of the cavernous sinus; and delimits the upper limit of the paraclival internal carotid artery (ICA) before the artery enters the cavernous sinus. The PPsb is anterior and medial to and below the sixth cranial nerve, forming the floor of Dorello’s canal. During surgery, gentle mobilization of the paraclival ICA reveals the petrosal process, serving as an accurate landmark for the location of the abducens nerve.

CONCLUSIONS

This investigation revealed details of the microsurgical anatomy of the PPsb, its anatomical relationships, and its application as a surgical landmark for identifying the abducens nerve. This novel landmark may help in minimizing the risk of abducens nerve injury during transclival approaches, which extend laterally toward the petrous apex and cavernous sinus region.