Microsurgical Anatomy of the Vertical Rami of the Superior Longitudinal Fasciculus: An Intraparietal Sulcus Dissection Study

Microsurgical Anatomy of the Vertical Rami of the Superior Longitudinal Fasciculus: An... Abstract BACKGROUND A number of vertical prolongations of the superior longitudinal fasciculus, which we refer to as the vertical rami (Vr), arise at the level of the supramarginal gyrus, directed vertically toward the parietal lobe. OBJECTIVE To provide the first published complete description of the white matter tracts (WMT) of the Vr, their relationship to the intraparietal and parieto-occipital sulci (IPS-POS complex), and their importance in neurosurgical approaches to the parietal lobe. METHODS Subcortical dissections of the Vr and WMT of the IPS were performed. Findings were correlated with a virtual dissection using high-resolution diffusion tensor imaging (DTI) tractography data derived from the Human Connectome Project. Example planning of a transparietal, transsulcal operative corridor is demonstrated using an integrated neuronavigation and optical platform. RESULTS The Vr were shown to contain component fibers of the superior longitudinal fasciculus (SLF)-II and SLF-III, with contributions from the middle longitudinal fasciculus merging into the medial bank of the IPS. The anatomic findings correlated well with DTI tractography. The line extending from the lateral extent of the POS to the IPS marks an ideal sulcal entry point that we have termed the IPS-POS Kassam-Monroy (KM) Point, which can be used to permit a safe parafascicular surgical trajectory to the trigone. CONCLUSION The Vr are a newly conceptualized group of tracts merging along the banks of the IPS, mediating connectivity between the parietal lobe and dorsal stream/SLF. We suggest a refined surgical trajectory to the ventricular atrium utilizing the posterior third of the IPS, at or posterior to the IPS-POS Point, in order to mitigate risk to the Vr and its considerable potential for postsurgical morbidity. Vertical rami, Superior longitudinal fasciculus, Intraparietal sulcus, Parieto-occipital sulcus, Parafascicular surgery, Transsulcal, DTI, Intraparietal Sulcus-Parieto-occipital Sulcus (IPS-POS) Point ABBREVIATIONS ABBREVIATIONS 3D three-dimensional AF arcuate fasciculus AG angular gyrus CR corona radiate CS centrum semiovale DTI diffusion tensor imaging IFOF inferior fronto-occipital fasciculus IPS-POS intraparietal sulcus-parieto-occipital sulcus IPL inferior parietal lobule IPS intraparietal sulcus IRC inner radial corridor KM kassam-monroy MdLF middle longitudinal fasciculus OR optic radiations ORC outer radial corridor POS parieto-occipital sulcus PTPA port-based transsulcal parafascicular approach ROVOT-m Robotically Operated Video Optical Telescopic Microscope platform SLF superior longitudinal fasciculus SMG supramarginal gyrus SPL superior parietal lobule Vr Vertical rami WMT white matter tract. The superior longitudinal fasciculus (SLF) is the longest dorsal frontoparietal white matter association tract, comprising 3 major subdivisions (SLF-I, SLF-II, and SLF-III). A vertical prolongation of the SLF arising at the level of the supramarginal gyrus and directed vertically toward the superior and inferior parietal lobules (SPL and IPL) has been largely neglected in the anatomic literature.1-4 We have consistently observed this collection of fibers (identified as blue fibers on RGB color-encoded diffusion tensor imaging (DTI) images given their rostro-caudal orientation) during the surgical planning and resection of parietal and periatrial brain tumors, and we have collectively termed these fibers the vertical rami (Vr). These fibers are thought to represent the terminations of the dorsal association tracts as they merge along the banks of the intraparietal sulcus (IPS) and form a rich subcortical network. Based on extensive study in the human and macaque, the IPS subcortical complex is thought to be a primary multisensory integration center governing functions such as spatial awareness, visuospatial attention, gaze, grasping, numerical cognition, and calculation.5 Apraxia, neglect, optic ataxia, and Gerstmann's and Balint's syndromes have been described as the result of parietal lobe dysfunction.6 By their close anatomic association with the IPS, we postulate that the Vr are in fact highly eloquent tracts from a neurosurgical perspective, serving to mediate connectivity between parietal lobe programs (such as praxis, visuospatial integration, attention, and numerical cognition) with motor and language programs residing in the dorsal processing stream (ie, the SLF). Given that the depth of the IPS is obliquely directed toward the roof of the atrium and the occipital horn,7,8 it is often used as a means of transparietal surgical access. However, controversy remains as to the ideal surgical corridor. Conventional parietal lobe approaches requiring a corticotomy, such as the transgyral approach, have the potential to damage the cortex and transect white matter tract (WMT), along with a greater risk of seizures. In addition, traditional approaches require a larger craniotomy and the use of retractors, which can result in brain injury. Indeed, a variety of postsurgical syndromes have been observed—right–left confusion, acalculia, agraphesthesia, agnosia, ideomotor apraxia, visual deficits—following IPS surgical approaches.9 However, newer, nearly “zero-footprint” techniques have been recently developed entailing port-based transsulcal parafascicular routes intended to prevent damage to the cortex and major WMT.10-13 The trajectory of the port, in this context, is planned as close to parallel as possible to the WMT fiber vectors as determined on DTI, so as to decrease the probability of transection of the subcortical U-fibers and major WMT en route to the atrium ventricular. Our goal was to define an optimized sulcal entry point and trajectory to the ventricular atrium. First, we sought to provide detailed microsurgical anatomic dissection study of the Vr in relation to the IPS-parieto-occipital sulci (POS) complex from cortex to atrium. We combined this with a “virtual dissection” based on high-resolution DTI data from the Human Connectome Project.16 On this basis, we describe a refined trajectory through the posterior third of the IPS near its intersection point with the lateral projection of the POS, which we term the IPS-POS (Kassam-Monroy) Point. In contrast to previously described access routes through the IPS, the IPS-POS (KM) Point marks the posterior extent of the IPS that can be used to permit a safe parafascicular surgical trajectory to the atrium/trigone, thus avoiding the Vr and its considerable potential for postsurgical morbidity. METHODS The study was conducted at the Surgical Neuroanatomy Laboratory. All research activities including clinical case review were authorized by our Institutional Review Board. Cadaveric Microsurgical Dissection One formalin-fixed cerebral hemisphere and 4 fully embalmed cadaveric human heads injected with red and blue silicon were studied. A standard microdissection of the relevant tracts was undertaken. Initially, the arachnoid, pia, and vessels were removed. All the cadaveric specimens were frozen for 2 wk at −15° C as part of a preparation previously described.14 The freezing stage facilitates the separation of gray and white matter with the formation of water crystals, causing space enlargement between the fibers, thereby facilitating easier dissection.15 The anatomic dissection of the IPS began by identifying the anatomic boundaries of the lateral parietal lobe. The length and depth of the IPS were measured with a digital caliper (Vernier Software & Technology, Beaverton, Oregon). We analyzed the IPS-POS complex in relation to the Vr according to 3 surgical-anatomic corridors: (1) Outer Radial Corridor (ORC), which contains bone, gyri, sulci, and vessels, (2) Inner Radial Corridor (IRC), which contains subcortical WMT, and (3) an oblique line of extension of the IPS to the lateral ventricle. Osseous landmarks (superior parietal line, coronal and lambdoid sutures) were studied in relationship to the junction of the sulcus of Jensen and the IPS, essentially creating external anatomic fiducials for trajectory planning. The WMT of the IPS complex were exposed in a stepwise manner, from lateral to medial and also from medial to lateral. These WMT in their respective orthogonal planes were identified, and their trajectories in relation with the Vr were analyzed. The atrium of the lateral ventricle marked the endpoint of the IPS complex. Finally, the BrainPath port device (NICO Corporation, Indianapolis, Indiana) was used with visualization provided by the Robotically Operated Video Optical Telescopic Microscope platform (ROVOT-m, Synaptive Medical, Toronto, Ontario) during the dissection in order to more closely simulate parafascicular surgery, demonstrating all WMT coaxial with the trajectory from IPS to the entry point into the atrium. All measurements are presented as the mean ± standard deviation (SD). High-Resolution DTI Tractography—Virtual Dissection We studied the white matter anatomy of the IPS-POS complex using a high-resolution DTI tractography “virtual dissection” technique. We utilized the open-source Human Connectome Project 7-Tesla multishell MRI-DTI data generated by the WU-Minnesota consortium.16 The HCP-842 atlas was constructed using a total of 842 subjects' diffusion MRI data from the Human Connectome Project (2015 Q4, 900-subject release).16 Diffusion images were acquired using a multishell diffusion scheme (b-values = 1000, 2000, and 3000 s/mm2, number of diffusion sampling directions = 90, 90, and 90, in-plane resolution = 1.25 mm, slice thickness = 1.25 mm). Diffusion data were reconstructed in the Montreal Neurological Institute (MNI) space using q-space diffeomorphic reconstruction to obtain the spin distribution function.17,18 A diffusion sampling length ratio of 1.25 was used, and the output resolution was 1 mm. The atlas was constructed by averaging the Synthetic Discriminant Functions (SDFs) of the 842 individual subjects. Tractography was accomplished using the open-source application DSI Studio (University of Pittsburgh [http://dsi-studio.labsolver.org], Pittsburgh, Pennsylvania). Tracts were manually seeded by 2 experienced neuroradiologists who placed the seed voxels and manually adjusted the tract density for each tract based on a priori tractography experience guided by the literature. Both neuroradiologists were blinded to the dissection data. The tracts reconstructed were arcuate fasciculus (AF), SLF-I, SLF-II, SLF-III, SLF-TP (temporoparietal projections of the SLF), middle longitudinal fasciculus (MdLF)-IPL and MdLF-SPL (MdLF fibers extending to the IPL and SPL, respectively), optic radiations (OR), cingulum, claustrocortical tracts, and corona radiate (CR). Three-dimensional (3D) renderings of the WMT were displayed in monocolor with a transparent overlay of the cortical gyri and sulci. Preoperative Planning Study Finally, the feasibility of a transsulcal port-based parafascicular approach was demonstrated by means of a clinical neurosurgical illustrative case. Clinical DTI images were acquired, and the surgical trajectory was planned using an integrated planning and neuronavigation system (Brightmatter Plan and Guide, Synaptive Medical, Toronto, Canada), according to methods previously reported by our group.18 RESULTS IPS Microsurgical Anatomic Dissection We consider the anatomic structures as an envelope guarding a central target, in this case the atrium. The corridor from the surface to the ventricle was divided into an ORC, consisting of soft-tissue, osseous structures, vessels, gyri, and sulci, and an IRC consisting of the cortical and subcortical neural network. The OR serves as the keystone functional WMT relevant to the transparietal approach to the atrium. ORC of the IPS-POS complex (Figure 1): Bone: In 8 hemispheres, the external cranial projection of the junction of the intermediate parietal sulcus of Jensen with the IPS was located on average 33.3 mm (SD = 0.94) anterior to the lambdoid suture, 27.1 mm (SD: 0.84) medial to the superior parietal line, and 24.1 mm (SD = 0.52) lateral to the sagittal suture. Vessels: The arteries of the IPS-POS complex are the anterior parietal artery, the posterior parietal artery and the angular artery. The veins present are the anterior parietal and posterior parietal veins. Gyri: The IPS separates the IPL (formed by the supramarginal gyrus (SMG) and angular gyrus (AG)) from the SPL. Sulci: IPS: The IPS is a deep sulcus arising from midpoint of the postcentral sulcus (ascending ramus) and initially coursing almost parallel to it. The IPS continues posteriorly running in a paramedian sagittal plane almost parallel with the interhemispheric fissure (horizontal ramus) towards the POS, where it joins with the intraoccipital sulcus situated in the occipital lobe. The IPS is delineated by (1) the postcentral sulcus anteriorly, (2) the vertical folds of Gromier, superficial or deep folds that are present along the pathway of the IPS, (3) the intermediate parietal sulcus of Jensen, directed inferiorly, (4) the Brissaud sulcus, directed toward the POS, and (5) the intraoccipital sulcus, an independent sulcus sometimes referred to as a branch of the IPS. The IPS was divided into anterior and posterior portions at the level of the sulcus of Jensen. The intermediate sulcus of Jensen separates the SMG from the AG and can be considered to be either an inferior vertical branch of the IPS, a distal and superior vertical branch of the superior temporal sulcus, or both.8 In 10 hemispheres, the mean length of the IPS was 43.8 mm (SD = 1.4), and its mean depth was 21.3 mm (SD = .79). The IPS was continuous in 6 hemispheres (60%) and in 4 hemispheres (40%) was separated by a gyral bridge. In the coronal plane, the IPS is obliquely rostro-caudally oriented running from superolateral to inferomedial with a deep trajectory extending towards the trigone. The atrium was situated deep to the anterior and posterior portions of the IPS; the occipital horn was related to the posterior third of the IPS. POS: The POS is one of the most important sulci in the medial surface of the hemisphere, separating the parietal lobe from the occipital lobe. It comprises 2 portions. The lateral portion is small, situated on the superolateral surface of the hemisphere between the SPL and occipital lobe, and oriented toward the posterior third of the IPS in close relation with lambdoid suture. The medial portion of the POS is long, oblique and deep, coursing along the mesial hemispheric surface anteriorly and inferiorly to join with the calcarine sulcus. IRC of the IPS-POS complex—Fiber Tracts (Figure 2 and Table 1): Following the removal of the cortex of the SMG/AG and SPL, the fiber tracts associated with the IPS were exposed. Dissection from lateral to medial identified: Dorsal AF: These fibers arise from the posterior part of the middle and inferior temporal gyri, passing under the angular gyrus and coursing posteriorly in a horizontal pathway deep to the lateral bank of the IPS, running ventral and lateral to the SLF-II, and finally directed anteriorly to the inferior and middle frontal gyri. As such, the fibers of the dorsal AF travel inferior, lateral, and parallel to the IPS, crossing underneath the Vr. SLF-II: This long association fiber tract runs beneath and parallel to the IPS, from the AG to the anterior and middle part of the middle frontal gyrus. With respect to the IPS, the SLF-II is situated deep and parallel to the sulcus at the level of the upper edge of the atrium and the occipital horn. SLF-III: This is an association fiber tract that connects the SMG to the pars opercularis, located lateral and inferior to the SLF-II. In the IPS complex, the SLF-III is situated parallel and lateral to the sulcus. It courses along the superolateral edge of the atrium of the lateral ventricle. Vr: These fiber bundles were consistently identified in all 10 hemispheres and are introduced here for the first time. The Vr were found to be situated in the anterior and middle thirds of the IPS complex, superior to and intermingled with the SLF-II. The Vr are the most superficial of the WMT located in the middle part of the IPS (after the U-fibers). They extend from the supramarginal gyrus to the IPL and SPL, connecting SLF-III through the SLF-II, coursing obliquely from inferior to superior, medial to lateral, and anterior to posterior. The average length of the Vr was 22.2 mm (SD = 0.22). MdLF: This tract extends from the temporal pole via the superior temporal gyrus with terminations in the SPL, IPL, and superior occipital lobule. The MdLF-SPL merges into the Vr along the medial bank of the IPS complex. The MdLF in the IPS is obliquely oriented in relation with the horizontal fibers of the SLF-II. The MdLF-IPL passes along the posterior third of the lateral wall and roof of the atrium and travels beneath the IPS, where it merges with the fibers of the inferior frontooccipital fasciculus (IFOF). IFOF: The IFOF is a long association tract that runs from the middle and inferior frontal gyri to the posterior parietal and occipital lobes. The posterior IFOF contributes to the sagittal stratum and is situated superficial and lateral to the posterior thalamic radiations, deep to the MdLF-IPL. The IFOF fibers passing deep to the IPS are almost vertically oriented, and are intimately related to the lateral wall of the atrium. Centrum semiovale (CS): The CS is situated under the cortex and continues ventrally as the CR. CS was observed deep to the IPS and is formed by SLF-II, parietal thalamic radiations and claustrocortical fibers. Tapetum: These fibers arise in the posterior body of the corpus callosum and splenium and sweep laterally and inferiorly to form the roof and lateral wall of the atrium, temporal, and occipital horn. The tapetum separates the fibers of the OR from the roof and lateral wall of the temporal horn and from the lateral wall of the atrium. After the tapetum was removed, the bulb and the calcar avis in the medial wall could then be observed, as well as the pulvinar in the anterior wall, the collateral trigone in the floor, and the connections with the temporal horn, occipital horn, and the body of the lateral ventricle. Forceps major: These callosal fibers arise from the splenium, forming an eminence in the upper part of the medial wall of the atrium and the occipital horn. As the forceps major sweeps posteriorly, its fibers join the posterior part of the IPS, directed in an oblique superior and posterior orientation to interconnect the occipital lobes. We can delimit a line of separation between the forceps major with the tapetum, which is located in the posterior ramus of the IPS; it represents the boundary between the medial wall and the roof of the atrium. Finally, we carried out a dissection from medial to lateral. The medial cortex of the superior frontal gyrus, paracentral lobule, precuneus, cingulum, and subsequently the U-projection fibers were removed, revealing the following (Figure 3): SLF-I: The first and most medial component of the SLF was found to extend from superior frontal gyrus (dorsal and medial cortex) to precuneus and SPL, forming connections through the supplementary motor areas, as described by others.1,4 Cingulum: The radiations of the cingulum directed toward the precuneus were situated inferior and medial to the SLF-I. Focusing mainly in the precuneus, the cingulum bundle was removed and we could observe the callosal fibers. The splenium and the posterior part of the body of the corpus callosum give rise to the tapetum and the forceps major. We could observe the callosal fibers and the parietal thalamic radiations between the SLF-I and the radiations of the cingulum alongside the Vr. Line of Extension and the IPS-POS Point (Figure 4) The line of extension is the deep projection of the IPS, extending through the WMT to the posterior body of the lateral ventricle, roof of the atrium, and occipital horn. This corridor was demonstrated using the BrainPath radial retractor/port system (Nico Corporation, Indianapolis, Indiana) that has a diameter of 13.5 mm. The most distal end of the port is 0.9 mm at its tip, which initially enters and engages the sulcus. The port then dilates the sulcus to a maximum diameter of 13.5 mm. Notably, the engagement point of the port was near the intersection of the IPS with the lateral line of projection of the convexity portion of the POS. This point we have termed the IPS-POS (Kassam-Monroy) Point and permits entry into a parafascicular zone leading to the atrium. This zone lies between SLF-II (laterally), and the projection fibers and SLF-I (medially), transecting the forceps major and extending superior and parallel to the oblique fibers of the MdLF-IPL and IFOF. Accessing the posterior third of the IPS in this fashion thus avoids the Vr. Additionally, we found that the OR lie primarily along the lateral wall of the atrium at this level, thus accessing the roof of the atrium does not transect visual fibers. FIGURE 1. View largeDownload slide ORC of the IPS complex is formed by osseous structures, vessels, gyri, and sulci. A, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with the IPS. B, The arteries present are the anterior parietal artery, the posterior parietal artery, and the angular artery. The veins presents are the anterior parietal and posterior parietal vein. C, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with respect to the junction of the intermediate parietal sulcus of Jensen and the IPS, also showing the convexity portion of the POS medially. D, Gyri around the IPS. E, Computer-rendered illustration further demonstrating the IPS-POS complex, the sulci of Jensen and Brissaud, and specifically the lateral projection line of the POS which intersects the IPS at the IPS-POS Point. Ang., angular; Ant., anterior; A., artery; Intrapar., intraparietal; Cent., central; Occip., occipital; Par., parietal; Post., posterior; Sag., sagittal; Sup., superior; Supramarg., supramarginal; Temp., temporal; V., vein; Vert., vertical. FIGURE 1. View largeDownload slide ORC of the IPS complex is formed by osseous structures, vessels, gyri, and sulci. A, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with the IPS. B, The arteries present are the anterior parietal artery, the posterior parietal artery, and the angular artery. The veins presents are the anterior parietal and posterior parietal vein. C, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with respect to the junction of the intermediate parietal sulcus of Jensen and the IPS, also showing the convexity portion of the POS medially. D, Gyri around the IPS. E, Computer-rendered illustration further demonstrating the IPS-POS complex, the sulci of Jensen and Brissaud, and specifically the lateral projection line of the POS which intersects the IPS at the IPS-POS Point. Ang., angular; Ant., anterior; A., artery; Intrapar., intraparietal; Cent., central; Occip., occipital; Par., parietal; Post., posterior; Sag., sagittal; Sup., superior; Supramarg., supramarginal; Temp., temporal; V., vein; Vert., vertical. FIGURE 2. View largeDownload slide Panoramic view of the lateral surface of the brain displaying the WMT of the Vr merging within the IPS. A, The cortex of the SPL, the supramarginal and angular gyri, and associated U-fibers have been removed to show the Vr from the SPL to the supramarginal gyrus, dividing the IPS in anterior and posterior part. Dotted line delineates the IPS. Anterior to the Vr is observed the SLF-II, and posteriorly the continuation of the SLF-II and AF dorsal segment. B, Focusing on the temporoparietal junction, the posterior part of the IPS (dotted line), the SLF-II and the AF dorsal segment were removed. The MdLF is observed to course obliquely, medial to the AF and SLF, merging within the middle portion of the Vr. C, The posterior part of the IPS (dotted line), was removed along with the MdLF revealing the superior fibers of the IFOF and the callosal fibers of the tapetum. Note how the ascending fibers of the SLF-II and SLF-III form a sling at the base of the anterior portion of the IPS, bridging from inferior to superior parietal lobe. D, High resolution DTI tractography simulates the view in C via a sagittal paramedian section (red dashed line, inset), showing in 3-dimensions the contributions of the SLF and MdLF to the Vr, and their relationship to the IFOF, corpus callosum and tapetum. FIGURE 2. View largeDownload slide Panoramic view of the lateral surface of the brain displaying the WMT of the Vr merging within the IPS. A, The cortex of the SPL, the supramarginal and angular gyri, and associated U-fibers have been removed to show the Vr from the SPL to the supramarginal gyrus, dividing the IPS in anterior and posterior part. Dotted line delineates the IPS. Anterior to the Vr is observed the SLF-II, and posteriorly the continuation of the SLF-II and AF dorsal segment. B, Focusing on the temporoparietal junction, the posterior part of the IPS (dotted line), the SLF-II and the AF dorsal segment were removed. The MdLF is observed to course obliquely, medial to the AF and SLF, merging within the middle portion of the Vr. C, The posterior part of the IPS (dotted line), was removed along with the MdLF revealing the superior fibers of the IFOF and the callosal fibers of the tapetum. Note how the ascending fibers of the SLF-II and SLF-III form a sling at the base of the anterior portion of the IPS, bridging from inferior to superior parietal lobe. D, High resolution DTI tractography simulates the view in C via a sagittal paramedian section (red dashed line, inset), showing in 3-dimensions the contributions of the SLF and MdLF to the Vr, and their relationship to the IFOF, corpus callosum and tapetum. FIGURE 3. View largeDownload slide Medial to lateral anatomic WMT dissection of the IPS-POS complex correlated with DTI rendering. A, Medial surface of the brain displaying the SLF-I and the prolongations of the cingulum bundle within the precuneus and also the relationships with the callosal fibers (tapetum and forceps major). B, Corresponding DTI rendering viewed from the medial side, depicting the relationship of the SLF-I, cingulum, and splenium. C, Superior view of the lateral (SPL) and medial (precuneus) surface of the brain shows the orientation of the Vr with respect to the SLF-I and the cingulum, which are separated by the CR and callosal fibers. D, Corresponding DTI tract rendering showing the Vr from this oblique posteromedial angle. Par. Occip, parieto-occipital; SLF., superior longitudinal fasciculus. FIGURE 3. View largeDownload slide Medial to lateral anatomic WMT dissection of the IPS-POS complex correlated with DTI rendering. A, Medial surface of the brain displaying the SLF-I and the prolongations of the cingulum bundle within the precuneus and also the relationships with the callosal fibers (tapetum and forceps major). B, Corresponding DTI rendering viewed from the medial side, depicting the relationship of the SLF-I, cingulum, and splenium. C, Superior view of the lateral (SPL) and medial (precuneus) surface of the brain shows the orientation of the Vr with respect to the SLF-I and the cingulum, which are separated by the CR and callosal fibers. D, Corresponding DTI tract rendering showing the Vr from this oblique posteromedial angle. Par. Occip, parieto-occipital; SLF., superior longitudinal fasciculus. FIGURE 4. View largeDownload slide Demonstration of the deep line of extension of the IPS leading to the atrium of the lateral ventricle. A, Superficial section showing the relevant gyral anatomy with simulated port access near the IPS-POS Point in the posterior third of the IPS. B, DTI rendering showing the relationship of the Vr to the access trajectory (white arrow). The Vr are clearly anterior to the approach vector, whereas the OR and IFOF remain lateral to this vector. C, The IPS has been further dissected showing the relationship of the Vr with the SLF-II. D, The surgical corridor developed from the posterior part of the IPS to the atrium can be organized as: (1) posterior to and parallel to the Vr; (2) posteromedial to the horizontally oriented SLF-II; (3) medial to the obliquely oriented dorsal AF; (4) superomedial to the OR passing along the lateral wall of the atrium; (5) posteromedial to the MdLF and IFOF having a direction that is almost vertical; and (6), oblique to the fibers of the tapetum. E, and F, Under vision with the ROVOT-m and using the port device, the callosal fibers were transected to see the ventricular atrium. AF., arcuate fasciculus; IFOF., Inferior frontooccipital fasciculus; MdLF., middle longitudinal fasciculus; Lat., lateral; Occip., occipital; SLF., superior longitudinal fasciculus; Temp., temporal; Vent., ventricle. FIGURE 4. View largeDownload slide Demonstration of the deep line of extension of the IPS leading to the atrium of the lateral ventricle. A, Superficial section showing the relevant gyral anatomy with simulated port access near the IPS-POS Point in the posterior third of the IPS. B, DTI rendering showing the relationship of the Vr to the access trajectory (white arrow). The Vr are clearly anterior to the approach vector, whereas the OR and IFOF remain lateral to this vector. C, The IPS has been further dissected showing the relationship of the Vr with the SLF-II. D, The surgical corridor developed from the posterior part of the IPS to the atrium can be organized as: (1) posterior to and parallel to the Vr; (2) posteromedial to the horizontally oriented SLF-II; (3) medial to the obliquely oriented dorsal AF; (4) superomedial to the OR passing along the lateral wall of the atrium; (5) posteromedial to the MdLF and IFOF having a direction that is almost vertical; and (6), oblique to the fibers of the tapetum. E, and F, Under vision with the ROVOT-m and using the port device, the callosal fibers were transected to see the ventricular atrium. AF., arcuate fasciculus; IFOF., Inferior frontooccipital fasciculus; MdLF., middle longitudinal fasciculus; Lat., lateral; Occip., occipital; SLF., superior longitudinal fasciculus; Temp., temporal; Vent., ventricle. TABLE 1. White Matter Tracts of the IPS-Complex—Vertical Ramia Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Bold text denotes putative components of the vertical rami (Vr) View Large TABLE 1. White Matter Tracts of the IPS-Complex—Vertical Ramia Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Bold text denotes putative components of the vertical rami (Vr) View Large DTI-Tractography Virtual Dissection DTI analysis reveals several important relationships with respect to the Vr. First, the Vr are clearly evident as medium-length, obliquely oriented, vertical rostro-caudal ramifications of the SLF, including contributions from both SLF-III and SLF-II as they terminate along the anterior two-thirds of the IPS. Along the medial aspect of the IPS, there are similar oblique fibers arising from the SLF-II and MdLF-SPL extending into the SPL, also along the anterior one-half to two-thirds of the IPS. Medial to these fibers are the claustrocortical tracts and CR, forming a densely anisotropic barrier between the cingulum and SLF-I located medially in the precuneus. Viewed in 3-dimensions, the components of the Vr take the form of a “sling” that cradles the anterior two-thirds of the IPS. However, the posterior third of the IPS is devoid of Vr fibers and thus serves as a potential subcortical keyhole corridor leading to the atrium of the lateral ventricle. When correlated with the surface anatomy, the IPS-POS (KM) Point represents an ideal surface landmark by which the proper trajectory can be engaged. This was confirmed with DTI virtual dissection and correlates exactly with the anatomic dissection findings—that is, a parafascicular trajectory affording minimal intersection of the surrounding WMT (Figure 5 and Video, Supplemental Digital Content 1). FIGURE 5. View largeDownload slide DTI virtual dissection correlating with parafasciular trajectory along IPS-POS complex. A, High resolution DTI global rendering of the left-hemispheric WMT relevant to the IPS-POS complex with transparent gyral overlay. Dotted line denotes the IPS. B, Inset demonstrates the ramifacations of the WMT in and around the IPS forming the Vr. Major contribution of the Vr comes from the SLF-II, with additional contributions from the SLF-III in the IPL as well as the MdLF in the SPL. SLF-I fibers are visible by way of removal of the overlying CR and corpus callosum tracts. Note the sling-like architecture of the Vr as they merge beneath and ramify on either side of the IPS. Color coding of white matter tracts: AF, teal; cingulum, orange; claustrocortical tract, magenta; CR, blue; Corpus callosum, red; SLF-I, light green; SLF-II, green; SLF-III, dark green; MdLF, white; SLF-temporoparietal fibers, yellow-green; OR, light blue. Lateral ventricle shown in dark blue in A. FIGURE 5. View largeDownload slide DTI virtual dissection correlating with parafasciular trajectory along IPS-POS complex. A, High resolution DTI global rendering of the left-hemispheric WMT relevant to the IPS-POS complex with transparent gyral overlay. Dotted line denotes the IPS. B, Inset demonstrates the ramifacations of the WMT in and around the IPS forming the Vr. Major contribution of the Vr comes from the SLF-II, with additional contributions from the SLF-III in the IPL as well as the MdLF in the SPL. SLF-I fibers are visible by way of removal of the overlying CR and corpus callosum tracts. Note the sling-like architecture of the Vr as they merge beneath and ramify on either side of the IPS. Color coding of white matter tracts: AF, teal; cingulum, orange; claustrocortical tract, magenta; CR, blue; Corpus callosum, red; SLF-I, light green; SLF-II, green; SLF-III, dark green; MdLF, white; SLF-temporoparietal fibers, yellow-green; OR, light blue. Lateral ventricle shown in dark blue in A. Illustrative Case We present a clinical case of a left trigonal intraventricular meningioma that was completely resected with a radial retractor/port. The surgical trajectory is demonstrated within the integrated Planning and Navigation software. Engagement was at the IPS-POS (KM) Point, and the parafascicular trajectory to the atrium via the posterior portion of the IPS is demonstrated (Figure 6, Video, Supplemental Digital Content 2). FIGURE 6. View largeDownload slide Transsulcal-parafascicular surgical trajectory for resection of intraventricular atrial meningioma. A, 3D surface rendering demonstrates the access engagement point utilizing the IPS-POS (Kassam-Monroy (KM)) Point. B, 3D graphical rendering of the IPS-POS Point that occurs at the junction of the POS and IPS. C, Sagittal planning view. Globally seeded tracts are rendered in RGB color-encoding within Brightmatter Plan (Synaptive Medical, Toronto, Ontario) integrated surgical planning and neuronavigation system. Access via the IPS-POS Point allows the device to pass posterior to the Vr within the posterior IPS, lateral to the cingulum, SLF-I and CR, above and medial to the IFOF and OR, and lateral to the SLF-II and SLF-III. Tumor is segmented in orange. D, Sagittal T2 FLAIR showed adjacent edema spreading to the OR. Postoperative axial E and sagittal F DTI imaging revealed gross total resection and minimal foot-print with complete preservation IFOF, OR, and Vr as shown in MR-DTI imaging. Of note, the patient did experience transient intraoperative deficits of visual spatial apraxia, agnosia, agraphesthesia, alexia, and left homonymous hemianopsia (all assessed by a board-certified neuro-ophthalmologist) that varied with the degree of manipulation of the port at the 9 o’clock position in relation to the Vr. During the follow-up visit (13 days postoperative), there were no deficits noted when examined by the same neuro-ophthalmologist. Also, formal visual fields were normal (shown in Video, Supplemental Digital Content 2). G, Anatomic dissection further demonstrating the “keyhole” extending to the atrium with port device in place. Red asterisk denotes the ventricular access point medial to the sagittal stratum containing the OR along the lateral wall of the atrium. H, High resolution DTI rendering of the parieto-occipital keyhole access module via the IPS-POS Point (denoted by red asterisk) at the posterior extent of the IPS (dotted green line). Note the position of the Vr, located superolateral to the trajectory, and the IFOF/OR located inferiorly. FIGURE 6. View largeDownload slide Transsulcal-parafascicular surgical trajectory for resection of intraventricular atrial meningioma. A, 3D surface rendering demonstrates the access engagement point utilizing the IPS-POS (Kassam-Monroy (KM)) Point. B, 3D graphical rendering of the IPS-POS Point that occurs at the junction of the POS and IPS. C, Sagittal planning view. Globally seeded tracts are rendered in RGB color-encoding within Brightmatter Plan (Synaptive Medical, Toronto, Ontario) integrated surgical planning and neuronavigation system. Access via the IPS-POS Point allows the device to pass posterior to the Vr within the posterior IPS, lateral to the cingulum, SLF-I and CR, above and medial to the IFOF and OR, and lateral to the SLF-II and SLF-III. Tumor is segmented in orange. D, Sagittal T2 FLAIR showed adjacent edema spreading to the OR. Postoperative axial E and sagittal F DTI imaging revealed gross total resection and minimal foot-print with complete preservation IFOF, OR, and Vr as shown in MR-DTI imaging. Of note, the patient did experience transient intraoperative deficits of visual spatial apraxia, agnosia, agraphesthesia, alexia, and left homonymous hemianopsia (all assessed by a board-certified neuro-ophthalmologist) that varied with the degree of manipulation of the port at the 9 o’clock position in relation to the Vr. During the follow-up visit (13 days postoperative), there were no deficits noted when examined by the same neuro-ophthalmologist. Also, formal visual fields were normal (shown in Video, Supplemental Digital Content 2). G, Anatomic dissection further demonstrating the “keyhole” extending to the atrium with port device in place. Red asterisk denotes the ventricular access point medial to the sagittal stratum containing the OR along the lateral wall of the atrium. H, High resolution DTI rendering of the parieto-occipital keyhole access module via the IPS-POS Point (denoted by red asterisk) at the posterior extent of the IPS (dotted green line). Note the position of the Vr, located superolateral to the trajectory, and the IFOF/OR located inferiorly. DISCUSSION The IPS-POS Complex The IPS and POS form an important sulcal complex along the respective lateral and medial surfaces of the parietal lobe harboring critical subcortical networks along their banks. We have recently published a conceptual framework to describe the subcortical white matter framework, the Surgical White Matter Chassis,19 which the reader may find useful in conceptualization of the IPS-POS complex. The Chassis is considered in 3 planes: median and paramedian planes, as well as an interconnecting network of oblique fascicles including the AF, uncinate fascicle, and Vr. Using this schema, the depth of the IPS corresponds to perhaps the most critical dorsal stream association bundle, namely the SLF, as it extends from the frontal to the occipital lobe. As the SLF traverses the parietal lobe, a connecting fiber network (Vr) emerges along an oblique rostro-caudal axis interconnecting SLF-II and III, bridging to the inner surface of the parietal lobe. We studied from a surgical view the intersection point of the sulcus of Jensen with the IPS in relationship with the superior temporal line, lambdoid suture and sagittal suture. We found that the cortico–subcortical relationship of the intersection point of the sulcus of Jensen with the IPS indeed corresponds to the position of the Vr. We further noted that the IPS sulcus was continuous in 60% and separated by a gyral bridge in 40%, with a recorded depth between a mean of 20 and 24 mm, in accordance with the literature.20-23 Accordingly, we report the IPS to have an average depth of 21.3 mm and length of 43.8 mm, divided into 2 main rami (anterior and posterior) by the sulcus of Jensen. Other landmarks have been previously established including the relationship of the IPS and postcentral sulcal intersection with the sagittal and lambdoid sutures,24 as well as the relationship between the superior temporal line with the IPS.25 From a functional standpoint, the neural networks terminating along the banks of the IPS, by way of their connectivity with the SLF, MdLF, and other dorsal stream pathways, are responsible for controlling various cognitive tasks including attention, spatial orientation and awareness, mental imagery, and working memory.26 Studies in the macaque have indicated that the IPS may harbor the following functional areas: (1) the lateral intraparietal area, activated in saccades and visual attention; (2) parietal reach region, involved in reaching arm movements; (3) anterior intraparietal area, activated for grasping activity; (4) caudal IPS, activated during grasping and discrimination of object size and orientation; and (5) ventral intraparietal area, activated to visual motion towards the face.9,27,28 In humans, neural networks associated with the anterior IPS are thought to process information related to high-level sensorimotor control, whereas those along the caudal IPS are thought to be related to visual-spatial attention processes.20 The Vertical Rami We here introduce the term “Vr” for the first time in order to collectively describe the bundle of ascending association fibers that connect the dorsal paramedian tracts, primarily the SLF-II and SLF-III, to the parietal lobe, terminating in and around the anterior and middle components of the IPS. To our knowledge, there has been no detailed anatomic or DTI study of these fibers with respect to the IPS-POS complex; this is particularly relevant given the access corridor the IPS provides to the atrium. We were able to observe the Vr in all of the imaging studies without difficulty; the Vr are superficial tracts located along the IPS composed primarily of SLF-II fibers, with lateral contributions from the SLF-III and medial contributions from the MdLF-SPL. Earlier DTI studies have described various temporoparietal fibers extending from the region of the AF/SLF complex extending to the IPL and SPL,29-31 thought to subserve critical speech, attentional and auditory localization functions. However, the exact relation of these fibers to the IPS was not elucidated. Fiber dissection and DTI studies have delineated the MdLF as extending primarily to the SPL along the medial bank of the IPS, with relatively few fibers extending into the IPL.32,33 Here, we find that these collective temporoparietal fiber bundles are indeed one and the same with the fibers that we describe as the Vr. Explicitly, these fibers represent the merging of SLF-II, SLF-III, SLF-TP, and MdLF fibers along the banks of the IPS. Based on our framework, we consider the Vr fibers to be critical oblique connections, articulating the major dorsal stream association fibers (ie, SLF) with the SPL. As such, the Vr are probably responsible for storing and accessing learned behavior within the parietal lobule; hence, disruption of these fibers is often associated with motor, sensory and special sensory apraxias and agnosias. The extent to which medial connectivity to the Vr exists (via SLF-I and cingulum) is uncertain. Kamali et al31 reported that the SLF-I originates in the superior and medial parietal cortex, in close proximity to the cingulum. A study of functional segregation within the frontoparietal networks demonstrated distinct dorsal spatial/motor and ventral nonspatial/motor networks associated with the SLF-II and III, respectively, whereas overlap of these functions was observed in the SLF-II.34 Similarly, our dissections demonstrated the connection of the SLF-III with the SLF-II, which merge within the Vr. When dissected from medial to lateral, we observed that the SLF-I and cingulum are situated medial to the Vr, separated by the CR and claustrocortical fibers. DTI did not reliably demonstrate any contributions of the SLF-I or cingulum to the Vr, possibly secondary to the difficulty in resolving crossing fibers. Any potential for a medial connection to the Vr will be an area of future investigation. Surgical Approach to the Trigone—Revised A decade ago, Ribas et al24 described the anterior IPS, namely its junction with the inferior frontal sulcus, as an ideal transparietal access target, based on anatomic dissection. A subsequent DTI study described a superficial “safe area” in the posterolateral parietal lobe yet concluded that there was no safe access to the atrium from this approach.35 Most recently, Koutsarnakis et al36 provide an excellent anatomic dissection study of the IPS and detailed discussion of the intraparietal approach with postsurgical deficits. The authors concluded that the mid-portion of the IPS is the ideal surgical access point; however, only the U-fibers, AF, CR, and tapetum were considered. Their conclusions are now challenged by the findings of our study—namely, the previously unreported existence of the Vr. The IPS has a short route to lesions situated in the posterior part of the body and atrium of the lateral ventricle,37,38 described here as the line of extension of the IPS corridor. The atrium is surrounded by a “node” of complex of neural structures—tapetum, OR, fibers of the internal capsule, SLF, MdLF, IFOF, CR, and AF—referred to as the temporoparietal fiber association area.39 The roof of the atrium is formed by the body, splenium, and tapetum of the corpus callosum. The tapetum separates the OR from the lateral wall of the atrium, as the posterior bundle of the OR passes lateral to the atrium to reach the calcarine sulcus.3,38,40 Indeed, the OR are at risk during transparietal and transtemporal approaches to the atrium.41 Mahaney et al40 claimed that a trajectory from the SPL to the trigone would traverse the OR. In the present study, however, we observed that the roof of the atrium is free of the OR, as also reported by others.3,4,38 Aside from small case series describing favorable outcomes with traditional trans-parietal approaches,37,42 larger case series have found that parietal lobe surgical approaches may result in surprisingly high rates of postoperative parietal apraxias, visual and language deficits, and up to an 8.4% incidence of permanent speech deficits.9 For this reason, our group has avoided the use of these classic mid- and anterior IPS approaches given the high risk to the Vr and potential for postsurgical deficits, primarily ideomotor and visual apraxias in our experience. Instead, we feel that the IPS-POS (Kassam-Monroy) Point described here represents a valid and potentially safer access point, resulting in a low posterolateral trajectory parallel to the Vr. Our group has had considerable success in using such a transsulcal trajectory through the posterior portion of the IPS. Such approaches are based on the groundwork laid by Yasargil,43 typically performed with a tubular retractor (port) system in conjunction with DTI-based planning and neuronavigation. Multiple centers have recently adopted and augmented this approach.10-13 Explicitly, if the coronally oriented POS is projected laterally to the intersection with the sagittally oriented IPS on the lateral surface; this marks the ideal portion of the IPS to access. The IPS-POS complex thus forms an equator curving along the posteromedial parieto-occipital convexity, along which there may be one or more suitable transsulcal access options for pathologies lateral (IPS) or medial (POS) to the OR. The further above this equator access is gained, the greater potential risk there exists to damage the Vr; the further below this equator, the greater risk there is to the OR and visual centers. Interestingly, this plane of access is in accordance to the anatomic plane of demarcation of fibers of the IFOF and claustrocortical system reported by Yagmurlu et al.3 In contrast, the sulcus of Jensen is a direct cortico–subcortical landmark for the Vr and thus should be avoided in any transsulcal approach. Limitations Dissection requires that the superficial WMT must be disrupted in order to visualize the deeper underlying tracts. Interobserver variability may occur based on the skill of the anatomist, fixation regimen, a priori assumptions of tract anatomy, and the particular microscopy technique utilized, and there may be difficulty in discerning parallel intermingling tracts. Conversely, DTI is subject to variability based on acquisition resolution, modeling assumptions, and choice of processing pipeline. The choice of seeding voxels is inherently subjective given that the ground truth of each tract is not entirely known. Anomalies can arise in the tractography when crossing, sharply angulating, or kissing fibers exist within a voxel. For our virtual dissection, we chose to utilize arguably the highest quality high-resolution DTI dataset available today, averaged among hundreds of subjects, to most faithfully generate ground truth tracts. To overcome some of the limitations of ROI-based tract seeding, we employ a global seeding pipeline within our presurgical planning system. Combining both dissection and DTI data should theoretically compensate for the limitations unique to each. CONCLUSION The Vr of the SLF, here conceptualized for the first time, can thus be thought of as an “interconnecting cable” allowing the generalized motor, cognitive, sensory, special sensory, and language pipelines of the dorsal processing stream to access the specialized multisensory integration programs of the parietal lobe. Considering this, we describe what we believe to be the ideal transsulcal trajectory to access subcortical lesions of the parietal lobe, achieved by engaging the IPS-POS (Kassam-Monroy) Point via the posterior third of the IPS en route to the ventricle. Although supported by our anatomic–radiologic correlation and surgical experience, further prospective analysis is now required. Thus, lays the keystone for the creation of modular, nearly “zero-footprint” surgical trajectories to lesions within the parietal and occipital lobes. Disclosures This research is supported by an award to the Aurora Research Institute by the Vince Lombardi Cancer Foundation. We would like to thank Nico Corporation, Carl Zeiss, Synaptive Medical, Stryker Medical, and Karl Storz for their donations that made our research possible in the Neuroanatomy Laboratory. 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Approaching the atrium through the intraparietal sulcus: mapping the sulcal morphology and correlating the surgical corridor to underlying fiber tracts . Oper Neurosurg 2017 ; 13 (4) : 503 – 516 . Google Scholar CrossRef Search ADS 37. Faquini I , Fonseca RB , Vale de Melo SL et al. Trigone ventricular meningiomas: is it possible to achieve good results even in the absence of high tech tools? Surg Neurol Int . 2015 ; 6 ( 1 ): 503 – 516 . 38. Kawashima M , Li X , Rhoton AL Jr , Ulm AJ , Oka H , Fujii K . Surgical approaches to the atrium of the lateral ventricle: microsurgical anatomy . Surg Neurol . 2006 ; 65 ( 5 ): 436 – 445 . Google Scholar CrossRef Search ADS PubMed 39. Martino J , da Silva-Freitas R , Caballero H , Marco de Lucas E , García-Porrero JA , Vázquez-Barquero A . Fiber dissection and diffusion tensor imaging tractography study of the temporoparietal fiber intersection area . Neurosurgery . 2013 ; 72 ( 1 Suppl Operative ): 87 – 97 . Google Scholar PubMed 40. Mahaney KB , Abdulrauf SI . Anatomic relationship of the optic radiations to the atrium of the lateral ventricle: description of a novel entry point to the trigone . Neurosurgery . 2008 ; 63 ( 4 Suppl 2 ): 195 – 202 . Google Scholar PubMed 41. Nayar VV , DeMonte F , Yoshor D , Blacklock JB , Sawaya R . Surgical approaches to meningiomas of the lateral ventricles . Clin Neurol Neurosurg . 2010 ; 112 ( 5 ): 400 – 405 . Google Scholar CrossRef Search ADS PubMed 42. Silva DO , Matis GK , Costa LF , Kitamura MA , Birbilis TA , Azevedo Filho HR . Intraventricular trigonal meningioma: neuronavigation? No, thanks! Surg Neurol Int . 2011 ; 2 ( 1 ): 1 – 13 . Google Scholar CrossRef Search ADS PubMed 43. Yasargil MG . A legacy of microneurosurgery: memoirs, lessons, and axioms . Neurosurgery . 1999 ; 45 ( 5 ): 1025 – 1092 . Google Scholar CrossRef Search ADS PubMed Supplemental digital content is available for this article at www.operativeneurosurgery-online.com. Supplemental Digital Content 1. Video. High resolution DTI of IPS-POS complex in the vertical rami of the SLF. HR-DTI virtual dissection of the tracts relevant to the IPS, with emphasis on the Vr of the SLF and MdLF, sequential build-up of tractography with multiangle 3-D rendering. Supplemental Digital Content 2. Video. Clinical case example, 3D DTI planning, and intraoperative surgical navigation. Example OR planning/neuronavigation case and intraoperative surgical resection using simultaneous navigation and a coregistered port. The video demonstrates the preoperative planning stages for this patient with special focus on the MR-DTI imaging and 3D rendering to calibrate port engagement in relation to the lateral projection of the POS and IPS—the IPS-POS Point—and posterior to the Vr. The surgery was performed under awake anesthesia with dynamic neurological cognitive and functional testing. Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Microsurgical Anatomy of the Vertical Rami of the Superior Longitudinal Fasciculus: An Intraparietal Sulcus Dissection Study

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Congress of Neurological Surgeons
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Copyright © 2018 by the Congress of Neurological Surgeons
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2332-4252
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2332-4260
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10.1093/ons/opy077
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Abstract

Abstract BACKGROUND A number of vertical prolongations of the superior longitudinal fasciculus, which we refer to as the vertical rami (Vr), arise at the level of the supramarginal gyrus, directed vertically toward the parietal lobe. OBJECTIVE To provide the first published complete description of the white matter tracts (WMT) of the Vr, their relationship to the intraparietal and parieto-occipital sulci (IPS-POS complex), and their importance in neurosurgical approaches to the parietal lobe. METHODS Subcortical dissections of the Vr and WMT of the IPS were performed. Findings were correlated with a virtual dissection using high-resolution diffusion tensor imaging (DTI) tractography data derived from the Human Connectome Project. Example planning of a transparietal, transsulcal operative corridor is demonstrated using an integrated neuronavigation and optical platform. RESULTS The Vr were shown to contain component fibers of the superior longitudinal fasciculus (SLF)-II and SLF-III, with contributions from the middle longitudinal fasciculus merging into the medial bank of the IPS. The anatomic findings correlated well with DTI tractography. The line extending from the lateral extent of the POS to the IPS marks an ideal sulcal entry point that we have termed the IPS-POS Kassam-Monroy (KM) Point, which can be used to permit a safe parafascicular surgical trajectory to the trigone. CONCLUSION The Vr are a newly conceptualized group of tracts merging along the banks of the IPS, mediating connectivity between the parietal lobe and dorsal stream/SLF. We suggest a refined surgical trajectory to the ventricular atrium utilizing the posterior third of the IPS, at or posterior to the IPS-POS Point, in order to mitigate risk to the Vr and its considerable potential for postsurgical morbidity. Vertical rami, Superior longitudinal fasciculus, Intraparietal sulcus, Parieto-occipital sulcus, Parafascicular surgery, Transsulcal, DTI, Intraparietal Sulcus-Parieto-occipital Sulcus (IPS-POS) Point ABBREVIATIONS ABBREVIATIONS 3D three-dimensional AF arcuate fasciculus AG angular gyrus CR corona radiate CS centrum semiovale DTI diffusion tensor imaging IFOF inferior fronto-occipital fasciculus IPS-POS intraparietal sulcus-parieto-occipital sulcus IPL inferior parietal lobule IPS intraparietal sulcus IRC inner radial corridor KM kassam-monroy MdLF middle longitudinal fasciculus OR optic radiations ORC outer radial corridor POS parieto-occipital sulcus PTPA port-based transsulcal parafascicular approach ROVOT-m Robotically Operated Video Optical Telescopic Microscope platform SLF superior longitudinal fasciculus SMG supramarginal gyrus SPL superior parietal lobule Vr Vertical rami WMT white matter tract. The superior longitudinal fasciculus (SLF) is the longest dorsal frontoparietal white matter association tract, comprising 3 major subdivisions (SLF-I, SLF-II, and SLF-III). A vertical prolongation of the SLF arising at the level of the supramarginal gyrus and directed vertically toward the superior and inferior parietal lobules (SPL and IPL) has been largely neglected in the anatomic literature.1-4 We have consistently observed this collection of fibers (identified as blue fibers on RGB color-encoded diffusion tensor imaging (DTI) images given their rostro-caudal orientation) during the surgical planning and resection of parietal and periatrial brain tumors, and we have collectively termed these fibers the vertical rami (Vr). These fibers are thought to represent the terminations of the dorsal association tracts as they merge along the banks of the intraparietal sulcus (IPS) and form a rich subcortical network. Based on extensive study in the human and macaque, the IPS subcortical complex is thought to be a primary multisensory integration center governing functions such as spatial awareness, visuospatial attention, gaze, grasping, numerical cognition, and calculation.5 Apraxia, neglect, optic ataxia, and Gerstmann's and Balint's syndromes have been described as the result of parietal lobe dysfunction.6 By their close anatomic association with the IPS, we postulate that the Vr are in fact highly eloquent tracts from a neurosurgical perspective, serving to mediate connectivity between parietal lobe programs (such as praxis, visuospatial integration, attention, and numerical cognition) with motor and language programs residing in the dorsal processing stream (ie, the SLF). Given that the depth of the IPS is obliquely directed toward the roof of the atrium and the occipital horn,7,8 it is often used as a means of transparietal surgical access. However, controversy remains as to the ideal surgical corridor. Conventional parietal lobe approaches requiring a corticotomy, such as the transgyral approach, have the potential to damage the cortex and transect white matter tract (WMT), along with a greater risk of seizures. In addition, traditional approaches require a larger craniotomy and the use of retractors, which can result in brain injury. Indeed, a variety of postsurgical syndromes have been observed—right–left confusion, acalculia, agraphesthesia, agnosia, ideomotor apraxia, visual deficits—following IPS surgical approaches.9 However, newer, nearly “zero-footprint” techniques have been recently developed entailing port-based transsulcal parafascicular routes intended to prevent damage to the cortex and major WMT.10-13 The trajectory of the port, in this context, is planned as close to parallel as possible to the WMT fiber vectors as determined on DTI, so as to decrease the probability of transection of the subcortical U-fibers and major WMT en route to the atrium ventricular. Our goal was to define an optimized sulcal entry point and trajectory to the ventricular atrium. First, we sought to provide detailed microsurgical anatomic dissection study of the Vr in relation to the IPS-parieto-occipital sulci (POS) complex from cortex to atrium. We combined this with a “virtual dissection” based on high-resolution DTI data from the Human Connectome Project.16 On this basis, we describe a refined trajectory through the posterior third of the IPS near its intersection point with the lateral projection of the POS, which we term the IPS-POS (Kassam-Monroy) Point. In contrast to previously described access routes through the IPS, the IPS-POS (KM) Point marks the posterior extent of the IPS that can be used to permit a safe parafascicular surgical trajectory to the atrium/trigone, thus avoiding the Vr and its considerable potential for postsurgical morbidity. METHODS The study was conducted at the Surgical Neuroanatomy Laboratory. All research activities including clinical case review were authorized by our Institutional Review Board. Cadaveric Microsurgical Dissection One formalin-fixed cerebral hemisphere and 4 fully embalmed cadaveric human heads injected with red and blue silicon were studied. A standard microdissection of the relevant tracts was undertaken. Initially, the arachnoid, pia, and vessels were removed. All the cadaveric specimens were frozen for 2 wk at −15° C as part of a preparation previously described.14 The freezing stage facilitates the separation of gray and white matter with the formation of water crystals, causing space enlargement between the fibers, thereby facilitating easier dissection.15 The anatomic dissection of the IPS began by identifying the anatomic boundaries of the lateral parietal lobe. The length and depth of the IPS were measured with a digital caliper (Vernier Software & Technology, Beaverton, Oregon). We analyzed the IPS-POS complex in relation to the Vr according to 3 surgical-anatomic corridors: (1) Outer Radial Corridor (ORC), which contains bone, gyri, sulci, and vessels, (2) Inner Radial Corridor (IRC), which contains subcortical WMT, and (3) an oblique line of extension of the IPS to the lateral ventricle. Osseous landmarks (superior parietal line, coronal and lambdoid sutures) were studied in relationship to the junction of the sulcus of Jensen and the IPS, essentially creating external anatomic fiducials for trajectory planning. The WMT of the IPS complex were exposed in a stepwise manner, from lateral to medial and also from medial to lateral. These WMT in their respective orthogonal planes were identified, and their trajectories in relation with the Vr were analyzed. The atrium of the lateral ventricle marked the endpoint of the IPS complex. Finally, the BrainPath port device (NICO Corporation, Indianapolis, Indiana) was used with visualization provided by the Robotically Operated Video Optical Telescopic Microscope platform (ROVOT-m, Synaptive Medical, Toronto, Ontario) during the dissection in order to more closely simulate parafascicular surgery, demonstrating all WMT coaxial with the trajectory from IPS to the entry point into the atrium. All measurements are presented as the mean ± standard deviation (SD). High-Resolution DTI Tractography—Virtual Dissection We studied the white matter anatomy of the IPS-POS complex using a high-resolution DTI tractography “virtual dissection” technique. We utilized the open-source Human Connectome Project 7-Tesla multishell MRI-DTI data generated by the WU-Minnesota consortium.16 The HCP-842 atlas was constructed using a total of 842 subjects' diffusion MRI data from the Human Connectome Project (2015 Q4, 900-subject release).16 Diffusion images were acquired using a multishell diffusion scheme (b-values = 1000, 2000, and 3000 s/mm2, number of diffusion sampling directions = 90, 90, and 90, in-plane resolution = 1.25 mm, slice thickness = 1.25 mm). Diffusion data were reconstructed in the Montreal Neurological Institute (MNI) space using q-space diffeomorphic reconstruction to obtain the spin distribution function.17,18 A diffusion sampling length ratio of 1.25 was used, and the output resolution was 1 mm. The atlas was constructed by averaging the Synthetic Discriminant Functions (SDFs) of the 842 individual subjects. Tractography was accomplished using the open-source application DSI Studio (University of Pittsburgh [http://dsi-studio.labsolver.org], Pittsburgh, Pennsylvania). Tracts were manually seeded by 2 experienced neuroradiologists who placed the seed voxels and manually adjusted the tract density for each tract based on a priori tractography experience guided by the literature. Both neuroradiologists were blinded to the dissection data. The tracts reconstructed were arcuate fasciculus (AF), SLF-I, SLF-II, SLF-III, SLF-TP (temporoparietal projections of the SLF), middle longitudinal fasciculus (MdLF)-IPL and MdLF-SPL (MdLF fibers extending to the IPL and SPL, respectively), optic radiations (OR), cingulum, claustrocortical tracts, and corona radiate (CR). Three-dimensional (3D) renderings of the WMT were displayed in monocolor with a transparent overlay of the cortical gyri and sulci. Preoperative Planning Study Finally, the feasibility of a transsulcal port-based parafascicular approach was demonstrated by means of a clinical neurosurgical illustrative case. Clinical DTI images were acquired, and the surgical trajectory was planned using an integrated planning and neuronavigation system (Brightmatter Plan and Guide, Synaptive Medical, Toronto, Canada), according to methods previously reported by our group.18 RESULTS IPS Microsurgical Anatomic Dissection We consider the anatomic structures as an envelope guarding a central target, in this case the atrium. The corridor from the surface to the ventricle was divided into an ORC, consisting of soft-tissue, osseous structures, vessels, gyri, and sulci, and an IRC consisting of the cortical and subcortical neural network. The OR serves as the keystone functional WMT relevant to the transparietal approach to the atrium. ORC of the IPS-POS complex (Figure 1): Bone: In 8 hemispheres, the external cranial projection of the junction of the intermediate parietal sulcus of Jensen with the IPS was located on average 33.3 mm (SD = 0.94) anterior to the lambdoid suture, 27.1 mm (SD: 0.84) medial to the superior parietal line, and 24.1 mm (SD = 0.52) lateral to the sagittal suture. Vessels: The arteries of the IPS-POS complex are the anterior parietal artery, the posterior parietal artery and the angular artery. The veins present are the anterior parietal and posterior parietal veins. Gyri: The IPS separates the IPL (formed by the supramarginal gyrus (SMG) and angular gyrus (AG)) from the SPL. Sulci: IPS: The IPS is a deep sulcus arising from midpoint of the postcentral sulcus (ascending ramus) and initially coursing almost parallel to it. The IPS continues posteriorly running in a paramedian sagittal plane almost parallel with the interhemispheric fissure (horizontal ramus) towards the POS, where it joins with the intraoccipital sulcus situated in the occipital lobe. The IPS is delineated by (1) the postcentral sulcus anteriorly, (2) the vertical folds of Gromier, superficial or deep folds that are present along the pathway of the IPS, (3) the intermediate parietal sulcus of Jensen, directed inferiorly, (4) the Brissaud sulcus, directed toward the POS, and (5) the intraoccipital sulcus, an independent sulcus sometimes referred to as a branch of the IPS. The IPS was divided into anterior and posterior portions at the level of the sulcus of Jensen. The intermediate sulcus of Jensen separates the SMG from the AG and can be considered to be either an inferior vertical branch of the IPS, a distal and superior vertical branch of the superior temporal sulcus, or both.8 In 10 hemispheres, the mean length of the IPS was 43.8 mm (SD = 1.4), and its mean depth was 21.3 mm (SD = .79). The IPS was continuous in 6 hemispheres (60%) and in 4 hemispheres (40%) was separated by a gyral bridge. In the coronal plane, the IPS is obliquely rostro-caudally oriented running from superolateral to inferomedial with a deep trajectory extending towards the trigone. The atrium was situated deep to the anterior and posterior portions of the IPS; the occipital horn was related to the posterior third of the IPS. POS: The POS is one of the most important sulci in the medial surface of the hemisphere, separating the parietal lobe from the occipital lobe. It comprises 2 portions. The lateral portion is small, situated on the superolateral surface of the hemisphere between the SPL and occipital lobe, and oriented toward the posterior third of the IPS in close relation with lambdoid suture. The medial portion of the POS is long, oblique and deep, coursing along the mesial hemispheric surface anteriorly and inferiorly to join with the calcarine sulcus. IRC of the IPS-POS complex—Fiber Tracts (Figure 2 and Table 1): Following the removal of the cortex of the SMG/AG and SPL, the fiber tracts associated with the IPS were exposed. Dissection from lateral to medial identified: Dorsal AF: These fibers arise from the posterior part of the middle and inferior temporal gyri, passing under the angular gyrus and coursing posteriorly in a horizontal pathway deep to the lateral bank of the IPS, running ventral and lateral to the SLF-II, and finally directed anteriorly to the inferior and middle frontal gyri. As such, the fibers of the dorsal AF travel inferior, lateral, and parallel to the IPS, crossing underneath the Vr. SLF-II: This long association fiber tract runs beneath and parallel to the IPS, from the AG to the anterior and middle part of the middle frontal gyrus. With respect to the IPS, the SLF-II is situated deep and parallel to the sulcus at the level of the upper edge of the atrium and the occipital horn. SLF-III: This is an association fiber tract that connects the SMG to the pars opercularis, located lateral and inferior to the SLF-II. In the IPS complex, the SLF-III is situated parallel and lateral to the sulcus. It courses along the superolateral edge of the atrium of the lateral ventricle. Vr: These fiber bundles were consistently identified in all 10 hemispheres and are introduced here for the first time. The Vr were found to be situated in the anterior and middle thirds of the IPS complex, superior to and intermingled with the SLF-II. The Vr are the most superficial of the WMT located in the middle part of the IPS (after the U-fibers). They extend from the supramarginal gyrus to the IPL and SPL, connecting SLF-III through the SLF-II, coursing obliquely from inferior to superior, medial to lateral, and anterior to posterior. The average length of the Vr was 22.2 mm (SD = 0.22). MdLF: This tract extends from the temporal pole via the superior temporal gyrus with terminations in the SPL, IPL, and superior occipital lobule. The MdLF-SPL merges into the Vr along the medial bank of the IPS complex. The MdLF in the IPS is obliquely oriented in relation with the horizontal fibers of the SLF-II. The MdLF-IPL passes along the posterior third of the lateral wall and roof of the atrium and travels beneath the IPS, where it merges with the fibers of the inferior frontooccipital fasciculus (IFOF). IFOF: The IFOF is a long association tract that runs from the middle and inferior frontal gyri to the posterior parietal and occipital lobes. The posterior IFOF contributes to the sagittal stratum and is situated superficial and lateral to the posterior thalamic radiations, deep to the MdLF-IPL. The IFOF fibers passing deep to the IPS are almost vertically oriented, and are intimately related to the lateral wall of the atrium. Centrum semiovale (CS): The CS is situated under the cortex and continues ventrally as the CR. CS was observed deep to the IPS and is formed by SLF-II, parietal thalamic radiations and claustrocortical fibers. Tapetum: These fibers arise in the posterior body of the corpus callosum and splenium and sweep laterally and inferiorly to form the roof and lateral wall of the atrium, temporal, and occipital horn. The tapetum separates the fibers of the OR from the roof and lateral wall of the temporal horn and from the lateral wall of the atrium. After the tapetum was removed, the bulb and the calcar avis in the medial wall could then be observed, as well as the pulvinar in the anterior wall, the collateral trigone in the floor, and the connections with the temporal horn, occipital horn, and the body of the lateral ventricle. Forceps major: These callosal fibers arise from the splenium, forming an eminence in the upper part of the medial wall of the atrium and the occipital horn. As the forceps major sweeps posteriorly, its fibers join the posterior part of the IPS, directed in an oblique superior and posterior orientation to interconnect the occipital lobes. We can delimit a line of separation between the forceps major with the tapetum, which is located in the posterior ramus of the IPS; it represents the boundary between the medial wall and the roof of the atrium. Finally, we carried out a dissection from medial to lateral. The medial cortex of the superior frontal gyrus, paracentral lobule, precuneus, cingulum, and subsequently the U-projection fibers were removed, revealing the following (Figure 3): SLF-I: The first and most medial component of the SLF was found to extend from superior frontal gyrus (dorsal and medial cortex) to precuneus and SPL, forming connections through the supplementary motor areas, as described by others.1,4 Cingulum: The radiations of the cingulum directed toward the precuneus were situated inferior and medial to the SLF-I. Focusing mainly in the precuneus, the cingulum bundle was removed and we could observe the callosal fibers. The splenium and the posterior part of the body of the corpus callosum give rise to the tapetum and the forceps major. We could observe the callosal fibers and the parietal thalamic radiations between the SLF-I and the radiations of the cingulum alongside the Vr. Line of Extension and the IPS-POS Point (Figure 4) The line of extension is the deep projection of the IPS, extending through the WMT to the posterior body of the lateral ventricle, roof of the atrium, and occipital horn. This corridor was demonstrated using the BrainPath radial retractor/port system (Nico Corporation, Indianapolis, Indiana) that has a diameter of 13.5 mm. The most distal end of the port is 0.9 mm at its tip, which initially enters and engages the sulcus. The port then dilates the sulcus to a maximum diameter of 13.5 mm. Notably, the engagement point of the port was near the intersection of the IPS with the lateral line of projection of the convexity portion of the POS. This point we have termed the IPS-POS (Kassam-Monroy) Point and permits entry into a parafascicular zone leading to the atrium. This zone lies between SLF-II (laterally), and the projection fibers and SLF-I (medially), transecting the forceps major and extending superior and parallel to the oblique fibers of the MdLF-IPL and IFOF. Accessing the posterior third of the IPS in this fashion thus avoids the Vr. Additionally, we found that the OR lie primarily along the lateral wall of the atrium at this level, thus accessing the roof of the atrium does not transect visual fibers. FIGURE 1. View largeDownload slide ORC of the IPS complex is formed by osseous structures, vessels, gyri, and sulci. A, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with the IPS. B, The arteries present are the anterior parietal artery, the posterior parietal artery, and the angular artery. The veins presents are the anterior parietal and posterior parietal vein. C, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with respect to the junction of the intermediate parietal sulcus of Jensen and the IPS, also showing the convexity portion of the POS medially. D, Gyri around the IPS. E, Computer-rendered illustration further demonstrating the IPS-POS complex, the sulci of Jensen and Brissaud, and specifically the lateral projection line of the POS which intersects the IPS at the IPS-POS Point. Ang., angular; Ant., anterior; A., artery; Intrapar., intraparietal; Cent., central; Occip., occipital; Par., parietal; Post., posterior; Sag., sagittal; Sup., superior; Supramarg., supramarginal; Temp., temporal; V., vein; Vert., vertical. FIGURE 1. View largeDownload slide ORC of the IPS complex is formed by osseous structures, vessels, gyri, and sulci. A, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with the IPS. B, The arteries present are the anterior parietal artery, the posterior parietal artery, and the angular artery. The veins presents are the anterior parietal and posterior parietal vein. C, Osseous relationship of the superior temporal line, sagittal suture, and lambdoid suture with respect to the junction of the intermediate parietal sulcus of Jensen and the IPS, also showing the convexity portion of the POS medially. D, Gyri around the IPS. E, Computer-rendered illustration further demonstrating the IPS-POS complex, the sulci of Jensen and Brissaud, and specifically the lateral projection line of the POS which intersects the IPS at the IPS-POS Point. Ang., angular; Ant., anterior; A., artery; Intrapar., intraparietal; Cent., central; Occip., occipital; Par., parietal; Post., posterior; Sag., sagittal; Sup., superior; Supramarg., supramarginal; Temp., temporal; V., vein; Vert., vertical. FIGURE 2. View largeDownload slide Panoramic view of the lateral surface of the brain displaying the WMT of the Vr merging within the IPS. A, The cortex of the SPL, the supramarginal and angular gyri, and associated U-fibers have been removed to show the Vr from the SPL to the supramarginal gyrus, dividing the IPS in anterior and posterior part. Dotted line delineates the IPS. Anterior to the Vr is observed the SLF-II, and posteriorly the continuation of the SLF-II and AF dorsal segment. B, Focusing on the temporoparietal junction, the posterior part of the IPS (dotted line), the SLF-II and the AF dorsal segment were removed. The MdLF is observed to course obliquely, medial to the AF and SLF, merging within the middle portion of the Vr. C, The posterior part of the IPS (dotted line), was removed along with the MdLF revealing the superior fibers of the IFOF and the callosal fibers of the tapetum. Note how the ascending fibers of the SLF-II and SLF-III form a sling at the base of the anterior portion of the IPS, bridging from inferior to superior parietal lobe. D, High resolution DTI tractography simulates the view in C via a sagittal paramedian section (red dashed line, inset), showing in 3-dimensions the contributions of the SLF and MdLF to the Vr, and their relationship to the IFOF, corpus callosum and tapetum. FIGURE 2. View largeDownload slide Panoramic view of the lateral surface of the brain displaying the WMT of the Vr merging within the IPS. A, The cortex of the SPL, the supramarginal and angular gyri, and associated U-fibers have been removed to show the Vr from the SPL to the supramarginal gyrus, dividing the IPS in anterior and posterior part. Dotted line delineates the IPS. Anterior to the Vr is observed the SLF-II, and posteriorly the continuation of the SLF-II and AF dorsal segment. B, Focusing on the temporoparietal junction, the posterior part of the IPS (dotted line), the SLF-II and the AF dorsal segment were removed. The MdLF is observed to course obliquely, medial to the AF and SLF, merging within the middle portion of the Vr. C, The posterior part of the IPS (dotted line), was removed along with the MdLF revealing the superior fibers of the IFOF and the callosal fibers of the tapetum. Note how the ascending fibers of the SLF-II and SLF-III form a sling at the base of the anterior portion of the IPS, bridging from inferior to superior parietal lobe. D, High resolution DTI tractography simulates the view in C via a sagittal paramedian section (red dashed line, inset), showing in 3-dimensions the contributions of the SLF and MdLF to the Vr, and their relationship to the IFOF, corpus callosum and tapetum. FIGURE 3. View largeDownload slide Medial to lateral anatomic WMT dissection of the IPS-POS complex correlated with DTI rendering. A, Medial surface of the brain displaying the SLF-I and the prolongations of the cingulum bundle within the precuneus and also the relationships with the callosal fibers (tapetum and forceps major). B, Corresponding DTI rendering viewed from the medial side, depicting the relationship of the SLF-I, cingulum, and splenium. C, Superior view of the lateral (SPL) and medial (precuneus) surface of the brain shows the orientation of the Vr with respect to the SLF-I and the cingulum, which are separated by the CR and callosal fibers. D, Corresponding DTI tract rendering showing the Vr from this oblique posteromedial angle. Par. Occip, parieto-occipital; SLF., superior longitudinal fasciculus. FIGURE 3. View largeDownload slide Medial to lateral anatomic WMT dissection of the IPS-POS complex correlated with DTI rendering. A, Medial surface of the brain displaying the SLF-I and the prolongations of the cingulum bundle within the precuneus and also the relationships with the callosal fibers (tapetum and forceps major). B, Corresponding DTI rendering viewed from the medial side, depicting the relationship of the SLF-I, cingulum, and splenium. C, Superior view of the lateral (SPL) and medial (precuneus) surface of the brain shows the orientation of the Vr with respect to the SLF-I and the cingulum, which are separated by the CR and callosal fibers. D, Corresponding DTI tract rendering showing the Vr from this oblique posteromedial angle. Par. Occip, parieto-occipital; SLF., superior longitudinal fasciculus. FIGURE 4. View largeDownload slide Demonstration of the deep line of extension of the IPS leading to the atrium of the lateral ventricle. A, Superficial section showing the relevant gyral anatomy with simulated port access near the IPS-POS Point in the posterior third of the IPS. B, DTI rendering showing the relationship of the Vr to the access trajectory (white arrow). The Vr are clearly anterior to the approach vector, whereas the OR and IFOF remain lateral to this vector. C, The IPS has been further dissected showing the relationship of the Vr with the SLF-II. D, The surgical corridor developed from the posterior part of the IPS to the atrium can be organized as: (1) posterior to and parallel to the Vr; (2) posteromedial to the horizontally oriented SLF-II; (3) medial to the obliquely oriented dorsal AF; (4) superomedial to the OR passing along the lateral wall of the atrium; (5) posteromedial to the MdLF and IFOF having a direction that is almost vertical; and (6), oblique to the fibers of the tapetum. E, and F, Under vision with the ROVOT-m and using the port device, the callosal fibers were transected to see the ventricular atrium. AF., arcuate fasciculus; IFOF., Inferior frontooccipital fasciculus; MdLF., middle longitudinal fasciculus; Lat., lateral; Occip., occipital; SLF., superior longitudinal fasciculus; Temp., temporal; Vent., ventricle. FIGURE 4. View largeDownload slide Demonstration of the deep line of extension of the IPS leading to the atrium of the lateral ventricle. A, Superficial section showing the relevant gyral anatomy with simulated port access near the IPS-POS Point in the posterior third of the IPS. B, DTI rendering showing the relationship of the Vr to the access trajectory (white arrow). The Vr are clearly anterior to the approach vector, whereas the OR and IFOF remain lateral to this vector. C, The IPS has been further dissected showing the relationship of the Vr with the SLF-II. D, The surgical corridor developed from the posterior part of the IPS to the atrium can be organized as: (1) posterior to and parallel to the Vr; (2) posteromedial to the horizontally oriented SLF-II; (3) medial to the obliquely oriented dorsal AF; (4) superomedial to the OR passing along the lateral wall of the atrium; (5) posteromedial to the MdLF and IFOF having a direction that is almost vertical; and (6), oblique to the fibers of the tapetum. E, and F, Under vision with the ROVOT-m and using the port device, the callosal fibers were transected to see the ventricular atrium. AF., arcuate fasciculus; IFOF., Inferior frontooccipital fasciculus; MdLF., middle longitudinal fasciculus; Lat., lateral; Occip., occipital; SLF., superior longitudinal fasciculus; Temp., temporal; Vent., ventricle. TABLE 1. White Matter Tracts of the IPS-Complex—Vertical Ramia Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Bold text denotes putative components of the vertical rami (Vr) View Large TABLE 1. White Matter Tracts of the IPS-Complex—Vertical Ramia Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Lateral Medial SMG/AG IPS-IPL IPS-SPL Precuneus Association AF SLF-TP MdLF –IPLIFOF SLF-II SLF-III SLF-II MdLF-SPL Cg SLF-I Projection Claustro-cortical CROR Commissural Forceps Major Tapetum Bold text denotes putative components of the vertical rami (Vr) View Large DTI-Tractography Virtual Dissection DTI analysis reveals several important relationships with respect to the Vr. First, the Vr are clearly evident as medium-length, obliquely oriented, vertical rostro-caudal ramifications of the SLF, including contributions from both SLF-III and SLF-II as they terminate along the anterior two-thirds of the IPS. Along the medial aspect of the IPS, there are similar oblique fibers arising from the SLF-II and MdLF-SPL extending into the SPL, also along the anterior one-half to two-thirds of the IPS. Medial to these fibers are the claustrocortical tracts and CR, forming a densely anisotropic barrier between the cingulum and SLF-I located medially in the precuneus. Viewed in 3-dimensions, the components of the Vr take the form of a “sling” that cradles the anterior two-thirds of the IPS. However, the posterior third of the IPS is devoid of Vr fibers and thus serves as a potential subcortical keyhole corridor leading to the atrium of the lateral ventricle. When correlated with the surface anatomy, the IPS-POS (KM) Point represents an ideal surface landmark by which the proper trajectory can be engaged. This was confirmed with DTI virtual dissection and correlates exactly with the anatomic dissection findings—that is, a parafascicular trajectory affording minimal intersection of the surrounding WMT (Figure 5 and Video, Supplemental Digital Content 1). FIGURE 5. View largeDownload slide DTI virtual dissection correlating with parafasciular trajectory along IPS-POS complex. A, High resolution DTI global rendering of the left-hemispheric WMT relevant to the IPS-POS complex with transparent gyral overlay. Dotted line denotes the IPS. B, Inset demonstrates the ramifacations of the WMT in and around the IPS forming the Vr. Major contribution of the Vr comes from the SLF-II, with additional contributions from the SLF-III in the IPL as well as the MdLF in the SPL. SLF-I fibers are visible by way of removal of the overlying CR and corpus callosum tracts. Note the sling-like architecture of the Vr as they merge beneath and ramify on either side of the IPS. Color coding of white matter tracts: AF, teal; cingulum, orange; claustrocortical tract, magenta; CR, blue; Corpus callosum, red; SLF-I, light green; SLF-II, green; SLF-III, dark green; MdLF, white; SLF-temporoparietal fibers, yellow-green; OR, light blue. Lateral ventricle shown in dark blue in A. FIGURE 5. View largeDownload slide DTI virtual dissection correlating with parafasciular trajectory along IPS-POS complex. A, High resolution DTI global rendering of the left-hemispheric WMT relevant to the IPS-POS complex with transparent gyral overlay. Dotted line denotes the IPS. B, Inset demonstrates the ramifacations of the WMT in and around the IPS forming the Vr. Major contribution of the Vr comes from the SLF-II, with additional contributions from the SLF-III in the IPL as well as the MdLF in the SPL. SLF-I fibers are visible by way of removal of the overlying CR and corpus callosum tracts. Note the sling-like architecture of the Vr as they merge beneath and ramify on either side of the IPS. Color coding of white matter tracts: AF, teal; cingulum, orange; claustrocortical tract, magenta; CR, blue; Corpus callosum, red; SLF-I, light green; SLF-II, green; SLF-III, dark green; MdLF, white; SLF-temporoparietal fibers, yellow-green; OR, light blue. Lateral ventricle shown in dark blue in A. Illustrative Case We present a clinical case of a left trigonal intraventricular meningioma that was completely resected with a radial retractor/port. The surgical trajectory is demonstrated within the integrated Planning and Navigation software. Engagement was at the IPS-POS (KM) Point, and the parafascicular trajectory to the atrium via the posterior portion of the IPS is demonstrated (Figure 6, Video, Supplemental Digital Content 2). FIGURE 6. View largeDownload slide Transsulcal-parafascicular surgical trajectory for resection of intraventricular atrial meningioma. A, 3D surface rendering demonstrates the access engagement point utilizing the IPS-POS (Kassam-Monroy (KM)) Point. B, 3D graphical rendering of the IPS-POS Point that occurs at the junction of the POS and IPS. C, Sagittal planning view. Globally seeded tracts are rendered in RGB color-encoding within Brightmatter Plan (Synaptive Medical, Toronto, Ontario) integrated surgical planning and neuronavigation system. Access via the IPS-POS Point allows the device to pass posterior to the Vr within the posterior IPS, lateral to the cingulum, SLF-I and CR, above and medial to the IFOF and OR, and lateral to the SLF-II and SLF-III. Tumor is segmented in orange. D, Sagittal T2 FLAIR showed adjacent edema spreading to the OR. Postoperative axial E and sagittal F DTI imaging revealed gross total resection and minimal foot-print with complete preservation IFOF, OR, and Vr as shown in MR-DTI imaging. Of note, the patient did experience transient intraoperative deficits of visual spatial apraxia, agnosia, agraphesthesia, alexia, and left homonymous hemianopsia (all assessed by a board-certified neuro-ophthalmologist) that varied with the degree of manipulation of the port at the 9 o’clock position in relation to the Vr. During the follow-up visit (13 days postoperative), there were no deficits noted when examined by the same neuro-ophthalmologist. Also, formal visual fields were normal (shown in Video, Supplemental Digital Content 2). G, Anatomic dissection further demonstrating the “keyhole” extending to the atrium with port device in place. Red asterisk denotes the ventricular access point medial to the sagittal stratum containing the OR along the lateral wall of the atrium. H, High resolution DTI rendering of the parieto-occipital keyhole access module via the IPS-POS Point (denoted by red asterisk) at the posterior extent of the IPS (dotted green line). Note the position of the Vr, located superolateral to the trajectory, and the IFOF/OR located inferiorly. FIGURE 6. View largeDownload slide Transsulcal-parafascicular surgical trajectory for resection of intraventricular atrial meningioma. A, 3D surface rendering demonstrates the access engagement point utilizing the IPS-POS (Kassam-Monroy (KM)) Point. B, 3D graphical rendering of the IPS-POS Point that occurs at the junction of the POS and IPS. C, Sagittal planning view. Globally seeded tracts are rendered in RGB color-encoding within Brightmatter Plan (Synaptive Medical, Toronto, Ontario) integrated surgical planning and neuronavigation system. Access via the IPS-POS Point allows the device to pass posterior to the Vr within the posterior IPS, lateral to the cingulum, SLF-I and CR, above and medial to the IFOF and OR, and lateral to the SLF-II and SLF-III. Tumor is segmented in orange. D, Sagittal T2 FLAIR showed adjacent edema spreading to the OR. Postoperative axial E and sagittal F DTI imaging revealed gross total resection and minimal foot-print with complete preservation IFOF, OR, and Vr as shown in MR-DTI imaging. Of note, the patient did experience transient intraoperative deficits of visual spatial apraxia, agnosia, agraphesthesia, alexia, and left homonymous hemianopsia (all assessed by a board-certified neuro-ophthalmologist) that varied with the degree of manipulation of the port at the 9 o’clock position in relation to the Vr. During the follow-up visit (13 days postoperative), there were no deficits noted when examined by the same neuro-ophthalmologist. Also, formal visual fields were normal (shown in Video, Supplemental Digital Content 2). G, Anatomic dissection further demonstrating the “keyhole” extending to the atrium with port device in place. Red asterisk denotes the ventricular access point medial to the sagittal stratum containing the OR along the lateral wall of the atrium. H, High resolution DTI rendering of the parieto-occipital keyhole access module via the IPS-POS Point (denoted by red asterisk) at the posterior extent of the IPS (dotted green line). Note the position of the Vr, located superolateral to the trajectory, and the IFOF/OR located inferiorly. DISCUSSION The IPS-POS Complex The IPS and POS form an important sulcal complex along the respective lateral and medial surfaces of the parietal lobe harboring critical subcortical networks along their banks. We have recently published a conceptual framework to describe the subcortical white matter framework, the Surgical White Matter Chassis,19 which the reader may find useful in conceptualization of the IPS-POS complex. The Chassis is considered in 3 planes: median and paramedian planes, as well as an interconnecting network of oblique fascicles including the AF, uncinate fascicle, and Vr. Using this schema, the depth of the IPS corresponds to perhaps the most critical dorsal stream association bundle, namely the SLF, as it extends from the frontal to the occipital lobe. As the SLF traverses the parietal lobe, a connecting fiber network (Vr) emerges along an oblique rostro-caudal axis interconnecting SLF-II and III, bridging to the inner surface of the parietal lobe. We studied from a surgical view the intersection point of the sulcus of Jensen with the IPS in relationship with the superior temporal line, lambdoid suture and sagittal suture. We found that the cortico–subcortical relationship of the intersection point of the sulcus of Jensen with the IPS indeed corresponds to the position of the Vr. We further noted that the IPS sulcus was continuous in 60% and separated by a gyral bridge in 40%, with a recorded depth between a mean of 20 and 24 mm, in accordance with the literature.20-23 Accordingly, we report the IPS to have an average depth of 21.3 mm and length of 43.8 mm, divided into 2 main rami (anterior and posterior) by the sulcus of Jensen. Other landmarks have been previously established including the relationship of the IPS and postcentral sulcal intersection with the sagittal and lambdoid sutures,24 as well as the relationship between the superior temporal line with the IPS.25 From a functional standpoint, the neural networks terminating along the banks of the IPS, by way of their connectivity with the SLF, MdLF, and other dorsal stream pathways, are responsible for controlling various cognitive tasks including attention, spatial orientation and awareness, mental imagery, and working memory.26 Studies in the macaque have indicated that the IPS may harbor the following functional areas: (1) the lateral intraparietal area, activated in saccades and visual attention; (2) parietal reach region, involved in reaching arm movements; (3) anterior intraparietal area, activated for grasping activity; (4) caudal IPS, activated during grasping and discrimination of object size and orientation; and (5) ventral intraparietal area, activated to visual motion towards the face.9,27,28 In humans, neural networks associated with the anterior IPS are thought to process information related to high-level sensorimotor control, whereas those along the caudal IPS are thought to be related to visual-spatial attention processes.20 The Vertical Rami We here introduce the term “Vr” for the first time in order to collectively describe the bundle of ascending association fibers that connect the dorsal paramedian tracts, primarily the SLF-II and SLF-III, to the parietal lobe, terminating in and around the anterior and middle components of the IPS. To our knowledge, there has been no detailed anatomic or DTI study of these fibers with respect to the IPS-POS complex; this is particularly relevant given the access corridor the IPS provides to the atrium. We were able to observe the Vr in all of the imaging studies without difficulty; the Vr are superficial tracts located along the IPS composed primarily of SLF-II fibers, with lateral contributions from the SLF-III and medial contributions from the MdLF-SPL. Earlier DTI studies have described various temporoparietal fibers extending from the region of the AF/SLF complex extending to the IPL and SPL,29-31 thought to subserve critical speech, attentional and auditory localization functions. However, the exact relation of these fibers to the IPS was not elucidated. Fiber dissection and DTI studies have delineated the MdLF as extending primarily to the SPL along the medial bank of the IPS, with relatively few fibers extending into the IPL.32,33 Here, we find that these collective temporoparietal fiber bundles are indeed one and the same with the fibers that we describe as the Vr. Explicitly, these fibers represent the merging of SLF-II, SLF-III, SLF-TP, and MdLF fibers along the banks of the IPS. Based on our framework, we consider the Vr fibers to be critical oblique connections, articulating the major dorsal stream association fibers (ie, SLF) with the SPL. As such, the Vr are probably responsible for storing and accessing learned behavior within the parietal lobule; hence, disruption of these fibers is often associated with motor, sensory and special sensory apraxias and agnosias. The extent to which medial connectivity to the Vr exists (via SLF-I and cingulum) is uncertain. Kamali et al31 reported that the SLF-I originates in the superior and medial parietal cortex, in close proximity to the cingulum. A study of functional segregation within the frontoparietal networks demonstrated distinct dorsal spatial/motor and ventral nonspatial/motor networks associated with the SLF-II and III, respectively, whereas overlap of these functions was observed in the SLF-II.34 Similarly, our dissections demonstrated the connection of the SLF-III with the SLF-II, which merge within the Vr. When dissected from medial to lateral, we observed that the SLF-I and cingulum are situated medial to the Vr, separated by the CR and claustrocortical fibers. DTI did not reliably demonstrate any contributions of the SLF-I or cingulum to the Vr, possibly secondary to the difficulty in resolving crossing fibers. Any potential for a medial connection to the Vr will be an area of future investigation. Surgical Approach to the Trigone—Revised A decade ago, Ribas et al24 described the anterior IPS, namely its junction with the inferior frontal sulcus, as an ideal transparietal access target, based on anatomic dissection. A subsequent DTI study described a superficial “safe area” in the posterolateral parietal lobe yet concluded that there was no safe access to the atrium from this approach.35 Most recently, Koutsarnakis et al36 provide an excellent anatomic dissection study of the IPS and detailed discussion of the intraparietal approach with postsurgical deficits. The authors concluded that the mid-portion of the IPS is the ideal surgical access point; however, only the U-fibers, AF, CR, and tapetum were considered. Their conclusions are now challenged by the findings of our study—namely, the previously unreported existence of the Vr. The IPS has a short route to lesions situated in the posterior part of the body and atrium of the lateral ventricle,37,38 described here as the line of extension of the IPS corridor. The atrium is surrounded by a “node” of complex of neural structures—tapetum, OR, fibers of the internal capsule, SLF, MdLF, IFOF, CR, and AF—referred to as the temporoparietal fiber association area.39 The roof of the atrium is formed by the body, splenium, and tapetum of the corpus callosum. The tapetum separates the OR from the lateral wall of the atrium, as the posterior bundle of the OR passes lateral to the atrium to reach the calcarine sulcus.3,38,40 Indeed, the OR are at risk during transparietal and transtemporal approaches to the atrium.41 Mahaney et al40 claimed that a trajectory from the SPL to the trigone would traverse the OR. In the present study, however, we observed that the roof of the atrium is free of the OR, as also reported by others.3,4,38 Aside from small case series describing favorable outcomes with traditional trans-parietal approaches,37,42 larger case series have found that parietal lobe surgical approaches may result in surprisingly high rates of postoperative parietal apraxias, visual and language deficits, and up to an 8.4% incidence of permanent speech deficits.9 For this reason, our group has avoided the use of these classic mid- and anterior IPS approaches given the high risk to the Vr and potential for postsurgical deficits, primarily ideomotor and visual apraxias in our experience. Instead, we feel that the IPS-POS (Kassam-Monroy) Point described here represents a valid and potentially safer access point, resulting in a low posterolateral trajectory parallel to the Vr. Our group has had considerable success in using such a transsulcal trajectory through the posterior portion of the IPS. Such approaches are based on the groundwork laid by Yasargil,43 typically performed with a tubular retractor (port) system in conjunction with DTI-based planning and neuronavigation. Multiple centers have recently adopted and augmented this approach.10-13 Explicitly, if the coronally oriented POS is projected laterally to the intersection with the sagittally oriented IPS on the lateral surface; this marks the ideal portion of the IPS to access. The IPS-POS complex thus forms an equator curving along the posteromedial parieto-occipital convexity, along which there may be one or more suitable transsulcal access options for pathologies lateral (IPS) or medial (POS) to the OR. The further above this equator access is gained, the greater potential risk there exists to damage the Vr; the further below this equator, the greater risk there is to the OR and visual centers. Interestingly, this plane of access is in accordance to the anatomic plane of demarcation of fibers of the IFOF and claustrocortical system reported by Yagmurlu et al.3 In contrast, the sulcus of Jensen is a direct cortico–subcortical landmark for the Vr and thus should be avoided in any transsulcal approach. Limitations Dissection requires that the superficial WMT must be disrupted in order to visualize the deeper underlying tracts. Interobserver variability may occur based on the skill of the anatomist, fixation regimen, a priori assumptions of tract anatomy, and the particular microscopy technique utilized, and there may be difficulty in discerning parallel intermingling tracts. Conversely, DTI is subject to variability based on acquisition resolution, modeling assumptions, and choice of processing pipeline. The choice of seeding voxels is inherently subjective given that the ground truth of each tract is not entirely known. Anomalies can arise in the tractography when crossing, sharply angulating, or kissing fibers exist within a voxel. For our virtual dissection, we chose to utilize arguably the highest quality high-resolution DTI dataset available today, averaged among hundreds of subjects, to most faithfully generate ground truth tracts. To overcome some of the limitations of ROI-based tract seeding, we employ a global seeding pipeline within our presurgical planning system. Combining both dissection and DTI data should theoretically compensate for the limitations unique to each. CONCLUSION The Vr of the SLF, here conceptualized for the first time, can thus be thought of as an “interconnecting cable” allowing the generalized motor, cognitive, sensory, special sensory, and language pipelines of the dorsal processing stream to access the specialized multisensory integration programs of the parietal lobe. Considering this, we describe what we believe to be the ideal transsulcal trajectory to access subcortical lesions of the parietal lobe, achieved by engaging the IPS-POS (Kassam-Monroy) Point via the posterior third of the IPS en route to the ventricle. Although supported by our anatomic–radiologic correlation and surgical experience, further prospective analysis is now required. Thus, lays the keystone for the creation of modular, nearly “zero-footprint” surgical trajectories to lesions within the parietal and occipital lobes. Disclosures This research is supported by an award to the Aurora Research Institute by the Vince Lombardi Cancer Foundation. We would like to thank Nico Corporation, Carl Zeiss, Synaptive Medical, Stryker Medical, and Karl Storz for their donations that made our research possible in the Neuroanatomy Laboratory. 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Approaching the atrium through the intraparietal sulcus: mapping the sulcal morphology and correlating the surgical corridor to underlying fiber tracts . Oper Neurosurg 2017 ; 13 (4) : 503 – 516 . Google Scholar CrossRef Search ADS 37. Faquini I , Fonseca RB , Vale de Melo SL et al. Trigone ventricular meningiomas: is it possible to achieve good results even in the absence of high tech tools? Surg Neurol Int . 2015 ; 6 ( 1 ): 503 – 516 . 38. Kawashima M , Li X , Rhoton AL Jr , Ulm AJ , Oka H , Fujii K . Surgical approaches to the atrium of the lateral ventricle: microsurgical anatomy . Surg Neurol . 2006 ; 65 ( 5 ): 436 – 445 . Google Scholar CrossRef Search ADS PubMed 39. Martino J , da Silva-Freitas R , Caballero H , Marco de Lucas E , García-Porrero JA , Vázquez-Barquero A . Fiber dissection and diffusion tensor imaging tractography study of the temporoparietal fiber intersection area . Neurosurgery . 2013 ; 72 ( 1 Suppl Operative ): 87 – 97 . Google Scholar PubMed 40. 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Video. High resolution DTI of IPS-POS complex in the vertical rami of the SLF. HR-DTI virtual dissection of the tracts relevant to the IPS, with emphasis on the Vr of the SLF and MdLF, sequential build-up of tractography with multiangle 3-D rendering. Supplemental Digital Content 2. Video. Clinical case example, 3D DTI planning, and intraoperative surgical navigation. Example OR planning/neuronavigation case and intraoperative surgical resection using simultaneous navigation and a coregistered port. The video demonstrates the preoperative planning stages for this patient with special focus on the MR-DTI imaging and 3D rendering to calibrate port engagement in relation to the lateral projection of the POS and IPS—the IPS-POS Point—and posterior to the Vr. The surgery was performed under awake anesthesia with dynamic neurological cognitive and functional testing. Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Operative NeurosurgeryOxford University Press

Published: Jun 5, 2018

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