Abstract
The incorporation of DTI and 3D tractography into the surgical planning workflow has increased awareness of the impact of resection of subcortical pathology as well as extra-axial anterior skull base lesions on the neural network. The 3D perspective that tractography affords in understanding neural anatomy, preoperative planning, and intraoperative navigation has provided unprecedented focus on neural network (both white matter tract and cranial nerve) preservation. The 3D-rendered neural network fused with CTA, structural MRI, and fMRI has prompted reanalysis of both subcortical and skull base surgical algorithms and refinement of conventional surgical approaches. Increased conspicuity of the neural network and integration of tractography in subcortical and skull base surgery aids in corridor choice, intraoperative navigation, and resection with the goal of minimizing the surgical footprint and maximizing patients’ quality of life.
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Keywords
FormalPara Key Points-
DTI and 3D tractography has recently been implemented as a useful tool for the surgical planning workflow of subcortical pathology and extra-axial skull base lesions.
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With a focus on neural network (white matter tracts and cranial nerve) preservation, combined DTI/3D tractography algorithms could have a positive impact on corridor selection.
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Combination and incorporation of these algorithms, along with CTA, structural MRI, and fMRI, in the preoperative planning and intraoperative navigation protocol may minimize the surgical footprint and postoperative morbidity.
11.1 Introduction
Advanced imaging techniques including diffusion tensor imaging (DTI) and functional magnetic resonance imaging (fMRI) provide unprecedented anatomical mapping of eloquent white and grey matter to inform neurosurgical decision-making. Previously inaccessible lesions may be targeted and trajectories developed that minimize risk to critical areas of brain function . Coupled with awake craniotomy and direct electrical stimulation (DES), risks of permanent neurological deficit may be minimized and return to preoperative level of function hastened and optimized [1,2,3,4,5,6,7,8,9].
The availability of rapid, automated DTI processing to produce whole-brain tractography has changed the practice of neurosurgical trajectory planning to allow incorporation of both cortical and white matter eloquence in devising the optimal surgical approach. Previously, white matter tract anatomy was primarily viewed in two dimensions. Three dimensional (3D) tractography was available at select centers or required labor and time-intensive post-processing by a dedicated neuroradiologist.
Although primarily considered a tool for surgical planning of deep-seated or subcortical lesions, tractography has also informed the planning of anterior skull base lesions.
11.2 Planning
Surgical planning of subcortical, deep-seated, and skull base pathology requires an understanding of the anatomy major white matter tracts (WMTs) at risk in consideration of a surgical trajectory. The framework of major WMTs evaluated in neurosurgical planning may be conceptualized as a neuroanatomic “chassis” that guides decision-making [10].
In trajectory planning for subcortical and deep-seated lesions, the first question to ask after consideration of eloquent cortex is: Which major tracts are most at risk? A brief review of the white matter anatomic framework highlights those tracts. Although a short description is included, the figures tell the story. The next question is: How do we reduce risk? After reviewing the neuroanatomic framework of major white matter tracts, planning concepts designed to reduce risk will be discussed.
The tracts are grossly organized according to their functions as commissures (hemispheric connections); association (cortical connections); and projection (descending connections). 2D representations of DTI arbitrarily assign each of these a color according to directionality: commissures—transverse—red; association—anteroposterior—green; projection—craniocaudal—blue; this convention yields the familiar 2D red-green-blue (RGB) maps. The 2D representations, however, fail to provide the 3D neuroanatomic perspective essential to preoperative simulation and neurosurgical planning. Recently, whole-brain 3D atlases have emerged to illustrate the white matter tract anatomy in stunning detail, although this may be, frankly, overwhelming when planning neurosurgical approaches [11]. Previous work by our group describes the 3D surgical white matter chassis in detail [10]. This practical guide highlights the major white matter tracts that influence surgical trajectory planning, rather than providing an exhaustive atlas, and is summarized below, although the reader is referred to the reference for detailed discussion [10].
Echoing the concepts promoted in skull base surgical planning literature, it is useful, when initially learning the white matter tract anatomy , to consider the relationship of the major tracts in a few planes, namely median and paramedian planes in the sagittal orientation and dorsal and ventral planes in the cranio-caudal orientation (Figs. 11.1 and 11.2).
11.3 Practical 3D Major White Matter Tract Anatomy for Neurosurgical Planning
There are two planes. The median plane , at the level of the third ventricle, is formed by the cingulum bundle and the corpus callosum . The paramedian is located at the level of the external capsule/claustrum and is formed by two cranio-caudal planes. The cranio-caudal planes corresponding at level of the corpus callosum dorsally and the level of the insula ventrally.
The corona radiata (CR), is interposed between median and paramedian planes and encompass both ventral and dorsal planes by virtue of their course. CR contain fibers that are amalgamated in the internal capsule, with ascending and descending spinal cord components.
Anterior limb internal capsule incorporates thalamocortical and frontopontine fibers. Posterior limb internal capsule transmits motor signals from precentral gyrus as well as sensory information to postcentral gyrus. CST is the primary motor pathway, with contribution primarily from precentral gyrus, along with premotor, supplementary motor area (SMA) and parietal input.
11.3.1 The Median Plane
Corpus callosum: The C-shaped corpus callosum (CC) is the major commissure of the brain and serves as the primary scaffold around which the major white matter tract framework, or “chassis” is built. The CC connects right and left hemispheric neocortical networks and is integral to orchestrating bimanual sensorimotor tasks, auditory and visuomotor coordination, and cognition [12, 13]. It is organized from anterior to posterior according to: prefrontal; premotor, supplementary motor area; motor; sensory; parieto-temporo-occipital connections [14]. Injury to the corpus callosum may result in disconnection syndromes characterized by disordered bimanual coordination, sensory or cognitive integration [15].
Cingulum: The cingulum bundle (CB ) an association tract, lies superior to the corpus callosum, connecting the forebrain and septal area to the precuneus, hippocampus, and parahippocampal gyrus [16, 17]. The cingulum is an interface between the limbic system and neocortex and is a governor of limbic drives [12, 16, 17]. Its anterior portion is involved with self-control, awareness, memory, and problem solving [12, 18]. The posterior portion has a putative role in the default mode network. The default mode network is implicated in memory, appraising the environment, managing emotional input, and integrating emotion and cognition at rest [19,20,21,22,23,24].
Fornix: It connects the mammillary bodies with the hippocampal formation and lies inferior to the corpus callosum, coursing along the medial thalamus [16, 25]. Integral to memory, deficits associated with forniceal transgression include visuospatial and verbal memory impairment [25].
11.3.2 The Paramedian Plane
11.3.2.1 Dorsal Plane
Superior Longitudinal Fasciculus (SLF): The SLF is the largest dorsal association tract and may be the most critical to cognition and executive function, serving as a relay between the frontal lobe (prefrontal cortex and premotor cortex) and parietal lobe centers of praxis, initiation, and attention [26, 27]. Its three main subdivisions lie within the superior, middle, and inferior frontal gyri. The medial SLF I, contained in the superior frontal gyrus above the cingulum, is implicated in higher motor function and the supplementary motor area (SMA). The more lateral SLF II, within the middle frontal gyrus, connects frontal and parietal lobes to facilitate visuospatial attention and spatial awareness. SLF III, within the inferior frontal gyrus, is a key component of the dorsal language stream underpinning expressive language, including articulation (dominant hemisphere) and prosody and music processing (non-dominant hemisphere) [27]. Injury to the SLF may produce visuospatial and working memory dysfunction (non-dominant) and language deficits including dysgraphia (ventral) (dominant) [26,27,28,29,30,31,32].
Arcuate Fasciculus (AF): The arcuate fasciculus is sometimes considered a fasciculus distinct from SLF and will be discussed below.
11.3.2.2 Ventral Plane
Inferior fronto-occipital fasciculus (IFOF): It is the longest, association tract. In addition, it is considered a multi-function bundle with broad connectivity with inferior frontal language and occipital visual association area . It is an important component of the ventral language pathway involved in semantic speech processing and semantic working memory [18]. The long course of IFOF implies function in frontal language and visual association [10].
Inferior longitudinal fasciculus (ILF): It is involved in the ventral visual pathway, including visual discrimination, motion detection, face/color perception, and visuospatial processing. It may contribute to emotional and memory components of ventral visual stream.
It may also have a role in the ventral language stream (dominant) and nonverbal semantic processing (non-dominant) [33]. Injury to the ILF may result in disorders of visual perception and deficits in object naming [30, 34].
Optic radiations (OR): They constitute the deepest of the lateral white matter tracts, extending between the lateral geniculate nucleus, running parallel to the lateral ventricle along lateral wall and floor to the temporal tip, to the occipital calcarine cortex [35]. Meyer’s loop is formed by an enlargement of the inferior component of the OR in the middle and anterior thirds of the temporal white matter and extends anteriorly along the lateral wall of the temporal horn, then turns, at its tip, to course posteromedially to the geniculate body, just posterior to the UF [35]. Meyer’s loop is vulnerable, especially in temporal lobe approaches, and injury may result in contralateral upper quadrantanopia [35]. Fibers of the IFOF, ILF, and OR intermingle in the temporoparietal junction to form a broad band of white matter termed the sagittal stratum [36].
11.3.3 Connecting Dorsal and Ventral Streams
Uncinate fasciculus (UF): It is a U-shaped limbic association fiber that originates from the uncus and amygdala, extends through temporal stem, and splays into ventrolateral and medial branches in orbitofrontal cortex [36]. The UF has an important role in episodic memory and memory integration. The nondominant UF is implicated in emotional empathy [37]. It is also a component of the ventral language stream, involved in semantic processing, and auditory working memory, and sound recognition [18, 31]. Injury may result in behavioral changes, memory and language impairment, retrograde amnesia in trauma patients . It has a postulated role in schizophrenia [38].
Arcuate fasciculus (AF): It connects the ventrolateral prefrontal cortex with the superior temporal gyrus [26]. The dorsal AF is primarily involved with lexical and semantic language (meaning) processing. The ventral portion is ascribed to phonological language (motor) processing, although there is overlap with SLF III . AF injury is associated with phonologic dysfunction and conduction aphasia [30].
Vertical rami of SLF (Vr): The vertical rami of the SLF arises from SLF II and SLF III and courses to the supramarginal and angular gyri superomedially to the superior parietal lobule. They are implicated in learning new tasks and injury results in apraxias [39, 40].
11.4 Workflow in Preoperative Planning and Intraoperative Navigation Using White Matter Tractography
Initially, accurate geometric fit of the 3D tractography volume with the anatomic T1/T2-weighted images is evaluated and confirmed using quality assurance tools embedded in the integrated preoperative planning and intraoperative navigation solution (Synaptive Medical). Surgical trajectory planning is performed within BrightMatter Plan (Synaptive Medical) using an algorithm for either conventional or port-based access . At our institution, typically the neuroradiologist, embedded in the neurosciences service line, performs initial semiautomated segmentation of tumor, critical arterial and venous anatomy integral to planning, and relevant cranial nerves. Specific regions of greater tumor cellularity may be targeted based on low apparent diffusion coefficient values.
The globally seeded DTI streamlines are automatically rendered in 3D according to standard RGB color-encoding, which can be reoriented by the user and culled on a sliding scale, based on tract complexity, length, and direction, to aid in developing and simulating an optimal trajectory. Initial identification of tracts at risk is based on fundamental knowledge and assumptions regarding the structure and function of major fiber bundles, as outlined above, and informed by the extensive operative experience of the neurosurgical team. Often, previous DTI tractography, regionally-seeded during post-processing of functional magnetic resonance imaging (fMRI), and fMRI regions of cortical activation are merged with structural MRI sequences for cross-reference during planning to influence the selection of sulcal entry points and targets. Initial trajectories are based on key neural structures, following the tenet of avoiding crossing a nerve or major tract; subsequently, the 3D shape and orientation of the targeted resection volume, anatomy of critical vascular structures, osseous and superficial structures are considered in designing and refining the operative trajectory and craniotomy . Trajectory plans are further refined based on surgical nuances by the neurosurgeon and uploaded to the integrated neuronavigation system (BrightMatter Guide, Synaptive Medical). Operative trajectory-guided resection is augmented by superimposing the preoperative 3D tractography upon the actual trajectory in real time. The navigation system is also fully integrated into a robotically operated video optical telescopic-microscopy (exoscope) unit (Synaptive Medical). Awake surgical approaches are preferred to other types of anesthesia in order to allow real-time feedback of the functional impact of the planned surgical corridor and to minimize the operative footprint through continuous testing. We employ intraoperative neurophysiological monitoring with somatosensory evoked potentials and motor evoked potentials. When especially eloquent areas are deemed at-risk based on location or preoperative fMRI, direct electrocortical stimulation mapping may also be used. In general, however, for the many cases that traverse nonmotor/nonsensory pathways, we consider traditional stimulation and neurophysiological monitoring less reliable than awake, real-time assessment of neurocognitive function. Our preferred workflow is to employ varied neurocognitive monitoring of multiple functions intraoperatively, including the ability to initiate tasks, praxis, and language using standard exams by a neuropsychologist compared with the baseline preoperative exam. For example, during cases targeting dominant-hemisphere parietal lobe lesions with planned access through the parietooccipital or intraparietal sulcus, the intraoperative assessment includes simple math equations and ability to read presented words in order to monitor function of the vertical rami (Vr) of the superior longitudinal fasciculus (SLF; i.e., Gerstmann syndrome) [10, 40].
11.5 White Matter Tractography Integration into Subcortical Neurosurgical Planning
11.5.1 Reducing Risk in Subcortical Neurosurgical Trajectories
Despite its advantages, DTI has inherent limitations including those related to resolution, the ability to accurately identify crossing white matter tracts, integration into navigation systems [41,42,43,44]. The technical details of 3D tractography are beyond the scope of this chapter, but excellent reviews are available [43]. Our group uses an integrated planning system that provides automated generation of whole brain 3D tractography from 2D datasets using whole-brain global seeding (as opposed to regional seeding) using a deterministic fourth-order Runge–Kutta interpolator (unpublished technical white paper, Synaptive Medical, Toronto, ON, 2016).
The initial phase of neurosurgical planning involves assessing critical neural and vascular structures at risk. Review of local anatomy and understanding of its functional correlates informs discussion of surgical risks with the patient . DTI with 3D tractography are often used in combination with fMRI and awake craniotomy, sometimes with cortical stimulation to reduce risk. Although each of these tools has inherent limitations , the combination of modalities is designed to mitigate risk. One of the primary considerations in using white matter tractography in neurosurgical planning is to reduce deflection of the major white matter tracts at risk in approaching the sought-after lesion. This can be accomplished in three main ways. The first is to develop trajectory, constrained by an entry point and target, that grossly parallels the major white matter tracts at risk. The goal is to create a trajectory with an angle of 30 degrees or less to the primary white matter tract at risk; a perpendicular (90 degree) trajectory would create risk for tract transection. The second strategy for reducing tract deflection, and hopefully, the operative “footprint,” is to create a trajectory that considers the geometry of the lesion. If the lesion is oblong, for instance, then developing the trajectory along the long axis of the lesion will potentially reduce the mobility of resection, and distortion of adjacent white matter tracts, required along the corridor. The third concept that may minimize tract deflection is the use of radial retraction, which, as opposed to flat retractors, distributes the force of retraction equally around the perimeter of the operative bed [3, 5, 16, 40, 45]. This is accomplished routinely at our institution through the use of port-based planning and resection and is illustrated through case examples (Figs. 11.3–11.5).
11.6 Refining Previous Conventional Neurosurgical Approaches Based on 3D Tractography
As a result of our increased knowledge of white matter tract anatomy and its impact on neurosurgical outcomes, and our experience with an operative workflow that incorporates 3D tractography, we have modified several previous approaches to pathology in the frontal lobes, third ventricle, and peri-atrial region. Through a combination of painstaking cadaveric microsurgical dissections of white matter tract anatomy and radiologic and neuropsychological and neurosurgical correlation, we have observed that a more anterior, than Kocher’s point, approach through the SFS in order to access frontal lobe pathology results in potentially greater preservation of SFS and reduction of cognitive sequalae (Fig. 11.6) [43, 44]. In accessing third ventricular lesions, we have likewise augmented our approach in consideration of reducing the operative footprint and preserving SLF, FAT, and CC through a SFS, awake craniotomy approach [45]. In addition, through the same process, we have identified , reproducibly, the vertical rami of the SLF which are critical to praxis and have adapted a more superior engagement point when using an intraparietal sulcus approach to reach peri-atrial lesions (Fig. 11.7) [37].
11.7 White Matter Tractography Integration into Skull Base Neurosurgical Planning
Advanced imaging has increased awareness of neural network preservation. Although the primary focus of 3D tractography in neurosurgery has been for resection of subcortical lesions, we felt it useful to apply it to skull base planning,
Despite advances in preoperative imaging and intraoperative optical platforms, reported skull base surgery morbidity is primarily related to cranial nerve injury. Few series, however, report neurocognitive status before and after surgery. Improved postoperative neurocognitive function was reported by Liouta, et al., 2016 in a series of 54 anterior and middle cranial fossa as well as convexity meningiomas [46]. Deteriorated neurocognitive function, particularly in adaptive functioning, was observed postoperatively in a series of 70 cases of meningiomas involving ventromedial prefrontal cortex (vmPFC) [47]. In that series, the authors advocate for early resection of meningiomas affecting vmPFC. An argument may also be made to reduce manipulation of vmPFC and IFOF in the resection of anterior cranial base lesions. Despite their extra-axial location, lesions adjacent brain parenchyma may affect critical neural function, in addition to cranial nerve (CN) function , which garners more attention in the skull base, especially with respect to cognition and behavior. The Hopkins group correlated executive function deficits with decreased frontal white matter fractional anisotropy (FA) in Alzheimer disease and mild cognitive impairment which may be extrapolated to other causes of white matter injury [48].
Although extent of resection (EOR) and cranial neuropathies are frequently reported in case series, impact of anterior cranial base resections rarely assess the impact of resection on cognition, which is more difficult to evaluate. Few series report neurocognitive status before and after surgery, despite distortion of frontal lobe architecture by anterior cranial base lesions. Typically, a general appraisal of “mental status” is documented preoperatively. Those series that did assess cognition were divided on the benefits of surgery to cognitive performance, which may relate to lesion location (skull base worse than convexity outcome) or surgical approach.
We have implemented a preoperative workflow with routine tractography planning in anterior skull base approaches [49]. 3D tractography of the neural network fused with CTA/MRI has prompted a reanalysis of relevant anatomy and surgical algorithm (Fig. 11.8). Increased conspicuity of neural network and integration of tractography in skull base surgery has aided in surgical corridor choice, navigation, and resection at our institution.
What does 3D tractography add to skull base surgical planning and navigation? Our group has found that the increased conspicuity of white matter tracts and nerves has enhanced mapping of distorted anatomy. This has facilitated a reduction in tract manipulation, and, potentially, injury. In the setting of endonasal approaches, there has been a qualitative enhancement of the surgeon’s efficiency navigating deformed anatomy. With respect to transcranial and transfacial approaches, traditional approaches have been modified and refined with greater awareness of the impact of surgical manipulation on eloquent white matter tracts. In considering skull base planning, in addition to cranial nerves, the major white matter tracts of significance include: inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus (ILF), uncinate fasciculus (UF), corpus callosum (CC), and cingulum bundle (CB) [49]. The functional anatomy has been reviewed above.
11.8 Corridor Selection Algorithm
Our approach to skull base trajectory planning is based upon the concept of layered, circumferential corridors, leading to the target. These are developed primarily with the goal of reducing manipulation of key neural elements: cranial nerves and major white matter tracts. DTI is especially helpful in focusing on the anteromedial and anterolateral corridors, which are divided into dorsal and ventral components.
The corridor selection algorithm at our institution is based on:
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1.
Location of pathology
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2.
Relative position of the key components of the radial framework
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Outer: soft tissue and osseous
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Inner: vasculature and cranial nerves
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3.
Previous neurosurgical procedures and their impact on the corridor
Generally, the dorsal corridors contain lesions that are primarily dorsal and lateral to the cranial nerves and the ventral anteromedial corridor is generally used for lesions ventral and medial to cranial nerves. The anteromedial (AM) corridor is selected to access pathology medial to optic nerve (ON) and IFOF. The anterolateral (AL) corridor is used to access lesions lateral to the third cranial nerve (CN III) and IFOF. The remaining corridors are beyond the scope of this chapter. For more information, see the chapter of the “Surgical Radial Corridors”.
At our institution, we recently have planned over 100 skull base surgeries with the 3D tractography workflow outlined. Of the 100 cases, 66 were ventral corridors, accessed via the expanded endoscopic endonasal approach (EEA) and 34 were transfacial/transcranial approaches (Figs. 11.9 and 11.10). Overall, functional cranial nerve recovery or improvement was observed in approximately 90% of cases.
11.9 Conclusion
A better knowledge of the microsurgical anatomy of the white matter tracts and advances of the technology as MRI–DTI 3D-tractography have promoted our understanding of subcortical anatomy. Currently, tractography has also demonstrated utility in other pathologies as skull base tumors. Tractography needs to be used carefully due to its technical limitations, and as such, the architecture of the tracts and the functionality should be assessed with awake mapping techniques. We believe, however, that continued advances of MRI–DTI tractography technology in the future of will demonstrate improved anatomic accuracy and integration of the interconnectivity of the fibers .
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Fukui, M.B. et al. (2021). Integration of White Matter Tractography in Subcortical and Skull Base Neurosurgical Planning. In: Monroy-Sosa, A., Chakravarthi, S.S., de la Garza-Salazar, J.G., Meneses Garcia, A., Kassam, A.B. (eds) Principles of Neuro-Oncology. Springer, Cham. https://doi.org/10.1007/978-3-030-54879-7_11
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