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Microvascular anatomy of the medial temporal region

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

OBJECTIVE

The authors investigated the microvascular anatomy of the hippocampus and its implications for medial temporal tumor surgery. They aimed to reveal the anatomical variability of the arterial supply and venous drainage of the hippocampus, emphasizing its clinical implications for the removal of associated tumors.

METHODS

Forty-seven silicon-injected cerebral hemispheres were examined using microscopy. The origin, course, irrigation territory, spatial relationships, and anastomosis of the hippocampal arteries and veins were investigated. Illustrative cases of hippocampectomy for medial temporal tumor surgery are also provided.

RESULTS

The hippocampal arteries can be divided into 3 segments, the anterior (AHA), middle (MHA), and posterior (PHA) hippocampal artery complexes, which correspond to irrigation of the hippocampal head, body, and tail, respectively. The uncal hippocampal and anterior hippocampal-parahippocampal arteries contribute to the AHA complex, the posterior hippocampal-parahippocampal arteries serve as the MHA complex, and the PHA and splenial artery compose the PHA complex. Rich anastomoses between hippocampal arteries were observed, and in 11 (23%) hemispheres, anastomoses between each segment formed a complete vascular arcade at the hippocampal sulcus. Three veins were involved in hippocampal drainage—the anterior hippocampal, anterior longitudinal hippocampal, and posterior longitudinal hippocampal veins—which drain the hippocampal head, body, and tail, respectively, into the basal and internal cerebral veins.

CONCLUSIONS

An understanding of the vascular variability and network of the hippocampus is essential for medial temporal tumor surgery via anterior temporal lobectomy with amygdalohippocampectomy and transsylvian selective amygdalohippocampectomy. Stereotactic procedures in this region should also consider the anatomy of the vascular arcade at the hippocampal sulcus.

In Journal of Neurosurgery Volume 137: Issue 3 (Sep 2022)

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Microsurgical approaches to the cerebellar interpeduncular region: qualitative and quantitative analysis

Juan Leonardo Serrato-Avila, Juan Alberto Paz Archila, Marcos Devanir Silva da Costa, Paulo Ricardo Rocha, Sergio Ricardo Marques, Luis Otavio Carvalho de Moraes, Sergio Cavalheiro, Kaan Yağmurlu, Michael T. Lawton, and Feres Chaddad-Neto

OBJECTIVE

The cerebellar interpeduncular region (CIPR) is a gate for dorsolateral pontine and cerebellar lesions accessed through the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), or the subtemporal transtentorial approach (STa). The authors sought to compare the exposures of the CIPR region that each of these approaches provided.

METHODS

Three approaches were performed bilaterally in eight silicone-injected cadaveric heads. The working area, area of exposure, depth of the surgical corridor, length of the interpeduncular sulcus (IPS) exposed, and bridging veins were statistically studied and compared based on each approach.

RESULTS

The OTa provided the largest working area (1421 mm2; p < 0.0001) and the longest surgical corridor (6.75 cm; p = 0.0006). Compared with the SCITa, the STa provided a larger exposure area (249.3 mm2; p = 0.0148) and exposed more of the length of the IPS (1.15 cm; p = 0.0484). The most bridging veins were encountered with the SCITa; however, no significant differences were found between this approach and the other approaches (p > 0.05).

CONCLUSIONS

To reach the CIPR, the STa provided a more extensive exposure area and more linear exposure than did the SCITa. The OTa offered a larger working area than the SCIT and the STa; however, the OTa had the most extensive surgical corridor. These data may help neurosurgeons select the most appropriate approach for lesions of the CIPR.

In Journal of Neurosurgery Volume 136: Issue 5 (May 2022)

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Lack of somatotopy among corticospinal tract fibers passing through the primate craniovertebral junction and cervical spinal cord: pathoanatomical substrate of central cord syndrome and cruciate paralysis

Robert J. Morecraft, Kimberly S. Stilwell-Morecraft, Jizhi Ge, Alexander Kraskov, and Roger N. Lemon

OBJECTIVE

In some cases of incomplete cervical spinal cord injury (iSCI) there is marked paresis and dysfunction of upper-extremity movement but not lower-extremity movement. A continued explanation of such symptoms is a somatotopic organization of corticospinal tract (CST) fibers passing through the decussation at the craniovertebral junction (CVJ) and lateral CST (LCST). In central cord syndrome, it has been suggested that injury to the core of the cervical cord may include selective damage to medially located arm/hand LCST fibers, without compromising laterally located leg fibers. Because such somatotopic organization in the primate CST might contribute to the disproportionate motor deficits after some forms of iSCI, the authors made a systematic investigation of CST organization in the CVJ and LCST using modern neuroanatomical techniques.

METHODS

High-resolution anterograde tracers were used in 11 rhesus macaque monkeys to define the course of the corticospinal projection (CSP) through the CVJ and LCST from the arm/hand, shoulder, and leg areas of the primary motor cortex (M1). This approach labels CST fibers of all sizes, large and small, arising in these areas. The CSP from the dorsolateral and ventrolateral premotor cortex and supplementary motor area were also studied. A stereological approach was adapted to quantify labeled fiber distribution in 8 cases.

RESULTS

There was no evidence for somatotopic organization of CST fibers passing through the CVJ or contralateral LCST. Fiber labeling from each cortical representation was widespread throughout the CST at the CVJ and LCST and overlapped extensively with fibers from other representations. This study demonstrated no significant difference between medial versus lateral subsectors of the LCST in terms of number of fibers labeled from the M1 arm/hand area.

CONCLUSIONS

This investigation firmly rejects the concept of somatotopy among CST fibers passing through the CVJ and LCST, in contrast with the somatotopy in the cortex, corona radiata, and internal capsule. All CST fibers in the CVJ and LCST would thus appear to be equally susceptible to focal or diffuse injury, regardless of their cortical origin. The disproportionate impairment of arm/hand movement after iSCI must therefore be due to other factors, including greater dependence of hand/arm movements on the CST compared with the lower limb. The dispersed and intermingled nature of frontomotor fibers may be important in motor recovery after cervical iSCI.

In Journal of Neurosurgery Volume 136: Issue 5 (May 2022)

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Comparative analysis of the combined petrosal and the pretemporal transcavernous anterior petrosal approach to the petroclival region

Mohamed A. Labib, Xiaochun Zhao, Lena Mary Houlihan, Irakliy Abramov, Joshua S. Catapano, Komal Naeem, Mark C. Preul, A. Samy Youssef, and Michael T. Lawton

OBJECTIVE

The combined petrosal (CP) approach has been traditionally used to resect petroclival meningioma (PCM). The pretemporal transcavernous anterior petrosal (PTAP) approach has emerged as an alternative. A quantitative comparison of both approaches has not been made. This anatomical study compared the surgical corridors afforded by both approaches and identified key elements of the approach selection process.

METHODS

Twelve cadaveric specimens were dissected, and 10 were used for morphometric analysis. Groups A and B (n = 5 in each) underwent the CP and PTAP approaches, respectively. The area of drilled clivus, lengths of cranial nerves (CNs) II–X, length of posterior circulation vessels, surgical area of exposure of the brainstem, and angles of attack anterior and posterior to a common target were measured and compared.

RESULTS

The area of drilled clivus was significantly greater in group A than group B (mean ± SD 88.7 ± 17.1 mm2 vs 48.4 ± 17.9 mm2, p < 0.01). Longer segments of ipsilateral CN IV (52.4 ± 2.33 mm vs 46.5 ± 3.71 mm, p < 0.02), CN IX, and CN X (9.91 ± 3.21 mm vs 0.00 ± 0.00 mm, p < 0.01) were exposed in group A than group B. Shorter portions of CN II (9.31 ± 1.28 mm vs 17.6 ± 6.89 mm, p < 0.02) and V1 (26.9 ± 4.62 mm vs 32.4 ± 1.93 mm, p < 0.03) were exposed in group A than group B. Longer segments of ipsilateral superior cerebellar artery (SCA) were exposed in group A than group B (36.0 ± 4.91 mm vs 25.8 ± 3.55 mm, p < 0.02), but there was less exposure of contralateral SCA (0.00 ± 0.00 mm vs 7.95 ± 3.33 mm, p < 0.01). There was no statistically significant difference between groups with regard to the combined area of the exposed cerebral peduncles and pons (p = 0.75). Although exposure of the medulla was limited, group A had significantly greater exposure of the medulla than group B (p < 0.01). Finally, group A had a smaller anterior angle of attack than group B (24.1° ± 5.62° vs 34.8° ± 7.51°, p < 0.03).

CONCLUSIONS

This is the first study to quantitatively identify the advantages and limitations of the CP and PTAP approaches from an anatomical perspective. Understanding these data will aid in designing maximally effective yet minimally invasive approaches to PCM.

In Journal of Neurosurgery Volume 136: Issue 3 (Mar 2022)

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A subset of arachnoid granulations in humans drain to the venous circulation via intradural lymphatic vascular channels

Kaan Yağmurlu, Jennifer Sokolowski, Sauson Soldozy, Pedro Norat, Musa Çırak, Petr Tvrdik, Mark E. Shaffrey, and M. Yashar S. Kalani

OBJECTIVE

The discovery of dural lymphatics has spurred interest in the mechanisms of drainage of interstitial fluid from the CNS, the anatomical components involved in clearance of macromolecules from the brain, mechanisms of entry and exit of immune components, and how these pathways may be involved in neurodegenerative diseases and cancer metastasis. In this study the authors describe connections between a subset of arachnoid granulations (AGs) and the venous circulation via intradural vascular channels (IVCs), which stain positively with established lymphatic markers. The authors postulate that the AGs may serve as a component of the human brain’s lymphatic system.

METHODS

AGs and IVCs were examined by high-resolution dissection under stereoscope bilaterally in 8 fresh and formalin-fixed human cadaveric heads. The superior sagittal sinus (SSS) and adjacent dura mater were immunostained with antibodies against Lyve-1 (lymphatic marker), podoplanin (lymphatic marker), CD45 (panhematopoietic marker), and DAPI (nuclear marker).

RESULTS

AGs can be classified as intradural or interdural, depending on their location and site of drainage. Interdural AGs are distinct from the dura, adhere to arachnoid membranes, and occasionally open directly in the inferolateral wall or floor of the SSS, although some cross the infradural folds of the dura’s inner layer to meet with intradural AGs and IVCs. Intradural AGs are located within the leaflets of the dura. The total number of openings from the AGs, lateral lacunae, and cortical veins into the SSS was 45 ± 5.62 per head. On average each cadaveric head contained 6 ± 1.30 intradural AGs. Some intradural AGs do not directly open into the SSS and use IVCs to connect to the venous circulation. Using immunostaining methods, the authors demonstrate that these tubular channels stain positively with vascular and lymphatic markers (Lyve-1, podoplanin).

CONCLUSIONS

AGs consist of two subtypes with differing modes of drainage into the SSS. A subset of AGs located intradurally use tubular channels, which stain positively with vascular and lymphatic markers to connect to the venous lacunae and ultimately to the SSS. The present study suggests that AGs may function as a component of brain lymphatics. This finding has important clinical implications for cancer metastasis to and from the CNS and may shed light on mechanisms of altered clearance of macromolecules in the setting of neurodegenerative diseases.

In Journal of Neurosurgery Volume 136: Issue 3 (Mar 2022)

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Where the central canal begins: endoscopic in vivo description

Pierluigi Longatti, Alessandro Fiorindi, Elisabetta Marton, Francesco Sala, and Alberto Feletti

OBJECTIVE

Although evidence and descriptions of the central canal (CC) along the medulla oblongata and the spinal cord have been provided by several anatomical and radiological studies, a clear picture and assessment of the opening of the CC, or apertura canalis centralis (ACC), into the fourth ventricle is lacking, due to its submillimetric size and hidden position in the calamus scriptorius.

METHODS

The authors reviewed all of their cases in which patients underwent ventricular transaqueductal flexible endoscopic procedures and selected 44 cases in which an inspection of the region of the calamus scriptorius had been performed and was suitable for study inclusion. Patients were divided into different groups, based on the presence or absence of a chronic pathological process involving the fourth ventricle. In each case, the visual appearance of the opening of the CC of the ACC was classified as no evidence (A0), indirect evidence (A1), or clear evidence (A2). Morphometric measurements were inferred from surrounding structures and the size of surgical tools visible in the field.

RESULTS

The opening of the CC could be clearly observed in all cases (A1 4.5%, A2 95.5%). In normal cases, a lanceolate shape along the median sulcus was most frequently found, with an average size of 600 × 250 µm that became rounded and smaller in size in cases of hydrocephalus. The distance between the caudal margin of the ACC and the obex was about 1.8 mm in normal cases, 2.1 mm in cases of obstructive hydrocephalus, and 1 mm in cases of normal pressure hydrocephalus. The two wings of the area postrema, variable in size and shape, were sited just caudal to the opening.

CONCLUSIONS

A flexible scope inserted through the cerebral aqueduct can approach the hidden calamus scriptorius like a pen fits into an inkpot. With this privileged viewpoint, the authors provide for the first time, to their knowledge, a clear and novel vision of the opening of the CC in the fourth ventricle, along with the precise location of this tiny structure compared to other anatomical landmarks in the inferior triangle.

In Journal of Neurosurgery Volume 136: Issue 3 (Mar 2022)

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Coding cerebral bypasses: a proposed nomenclature to better describe bypass constructs and revascularization techniques

Ali Tayebi Meybodi, Arjun Gadhiya, Leandro Borba Moreira, and Michael T. Lawton

OBJECTIVE

Bypass surgery has evolved into a complex surgical art with a variety of donor arteries, recipient arteries, interpositional grafts, anastomoses, and suturing techniques. Although innovation in contemporary bypasses has increased, the literal descriptions of these new bypasses have not kept pace. The existing nomenclature that joins donor and recipient arteries with a hyphen is simplistic, underinformative, and in need of improvement. This article proposes a nomenclature that systematically incorporates anatomical and technical details with alphanumeric abbreviations and is a clear, concise, and practical “code” for bypass surgery.

METHODS

Detailed descriptions and illustrations of the proposed nomenclature, which consists of abbreviations for donor and recipient arteries, arterial segments, arteriotomies, and sides (left or right), with hyphens and parentheses to denote the arteriotomies joined in the anastomosis and brackets and other symbols for combination bypasses, are presented. The literature was searched for articles describing bypasses, and descriptive nomenclature was categorized as donor and recipient arteries (donor-recipient), donor-recipient with additional details, less detail than donor-recipient, and complete, ambiguous, or descriptive text.

RESULTS

In 483 publications, most bypass descriptions were categorized as donor-recipient (335, 69%), with superficial temporal artery–middle cerebral artery bypass described most frequently (299, 62%). Ninety-seven articles (20%) used donor-recipient descriptions with additional details, 45 (9%) were categorized as ambiguous, and none contained a complete bypass description. The authors found the proposed nomenclature to be easily applicable to the more complex bypasses reported in the literature.

CONCLUSIONS

The authors propose a comprehensive nomenclature based on segmental anatomy and additional anastomotic details that allows bypasses to be coded simply, succinctly, and accurately. This alphanumeric shorthand allows greater precision in describing bypasses and clarifying technical details, which may improve reporting in the literature and thus help to advance the field of bypass surgery.

In Journal of Neurosurgery Volume 136: Issue 1 (Jan 2022)

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Microsurgical anatomy of the lateral posterior choroidal artery: implications for intraventricular surgery involving the choroid plexus

Yuanzhi Xu, Ahmed Mohyeldin, Ayoze Doniz-Gonzalez, Vera Vigo, Felix Pastor-Escartin, Lingzhao Meng, Aaron A Cohen-Gadol, and Juan C Fernandez-Miranda

OBJECTIVE

The lateral posterior choroidal artery (LPChA) should be a major surgical consideration in the microsurgical management of lateral ventricular tumors. Here the authors aim to delineate the microsurgical anatomy of the LPChA by using anatomical microdissections. They describe the trajectory, segments, and variations of the LPChA and discuss the surgical implications when approaching the choroid plexus using different routes.

METHODS

Twelve colored silicone–injected, lightly fixed, postmortem human head specimens were prepared for dissection. The origin, diameter, trunk, course, segment, length, spatial relationships, and anastomosis of the LPChA were investigated. The surgical landmarks of 4 different approaches to the LPChA were also examined thoroughly.

RESULTS

The LPChA was present in 23 hemispheres (96%), and in 14 (61%) it originated from the posterior segment of the P2 (i.e., P2P); most commonly (61%) the LPChA had 2 trunks, and in 17 hemispheres (74%) it had a C-shaped trajectory. According to its course, the authors divided the LPChA into 3 segments: 1) cisternal, from PCA to choroidal fissure (length 10.6 ± 2.5 mm); 2) forniceal, starting at the choroidal fissure, 8.2 ± 5.7 mm posterior to the inferior choroidal point, and terminating at the posterior level of the choroidal fissure (length 28.7 ± 6.8 mm); and 3) pulvinar, starting at the posterior choroidal fissure and terminating in the pulvinar (length 5.9 ± 2.2 mm). The LPChA was divided into 3 patterns according to its entrance into the choroidal fissure: A (anterior) 78%; B (posterior) 13%; and C (mixed) 9%. The transsylvian trans–limen insulae approach provided the best exposure for cisternal and proximal forniceal segments; the lateral transtemporal approach facilitated a more direct approach to the forniceal segment, including cases with posterior entrance; the transparietal transcortical and contralateral posterior interhemispheric transfalcine transprecuneus approaches provided direct access to the pulvinar segment of the LPChA and to the posterior forniceal segment, including cases with posterior choroidal entrance.

CONCLUSIONS

The LPChA typically runs in the medial border of the choroid plexus, which may facilitate its recognition during surgery. The distance between the AChA at the inferior choroidal point and the LPChA is a valuable reference during surgery, but there are cases of posterior choroidal entrance. Most frequently, there are 2 or more LPChA trunks, which makes possible the sacrifice of one trunk feeding the tumor while preserving the other that provides supply to relevant structures. The intraventricular approaches can be selected based on the tumor location and the LPChA anatomy.

In Journal of Neurosurgery Volume 135: Issue 5 (Nov 2021)

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Composition and organization of the sagittal stratum in the human brain: a fiber dissection study

Igor Lima Maldonado, Christophe Destrieux, Eduardo Carvalhal Ribas, Bruna Siqueira de Abreu Brito Guimarães, Patrícia Pontes Cruz, and Hugues Duffau

OBJECTIVE

The sagittal stratum is divided into two layers. In classic descriptions, the stratum sagittale internum corresponds to optic radiations (RADs), whereas the stratum sagittale externum corresponds to fibers of the inferior longitudinal fasciculus. Although advanced for the time it was proposed, this schematic organization seems simplistic considering the recent progress on the understanding of cerebral connectivity and needs to be updated. Therefore, the authors sought to investigate the composition of the sagittal stratum and to detail the anatomical relationships among the macroscopic fasciculi.

METHODS

The authors performed a layer-by-layer fiber dissection from the superolateral aspect to the ventricular cavity in 20 cadaveric human hemispheres.

RESULTS

Diverse bundles of white matter were observed to contribute to the sagittal stratum and their spatial arrangement was highly consistent from one individual to another. This was the case of the middle longitudinal fasciculus, the inferior fronto-occipital fasciculus, the RADs, and other posterior thalamic radiations directed to nonvisual areas of the cerebral cortex. In addition, small contributions to the sagittal stratum came from the anterior commissure anteriorly and the inferior longitudinal fasciculus inferiorly.

CONCLUSIONS

A general model of sagittal stratum organization in layers is possible, but the composition of the external layer is much more complex than is mentioned in classic descriptions. A small contribution of the inferior longitudinal fasciculus is the main difference between the present results and the classic descriptions in which this bundle was considered to entirely correspond to the stratum sagittale externum. This subject has important implications both for fundamental research and neurosurgery, as well as for the development of surgical approaches for the cerebral parenchyma and ventricular system.

In Journal of Neurosurgery Volume 135: Issue 4 (Oct 2021)

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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 Volume 135: Issue 3 (Sep 2021)