3D Simulations of the White Matter Anatomy of the Cerebrum
BACKGROUND: An understanding of the anatomy of white matter tracts and their 3-dimensional (3D) relationship with each other is important for neurosurgical practice. The fiber dissection technique contributes to this understanding because it involves removing the brain's white matter tracts to reveal their anatomic organization. Using this technique, we built freely accessible 3D models and augmented and virtual reality simulations of white matter tracts.
OBJECTIVE: To define the white matter tracts of cadaveric human brains through fiber dissection and to make 2-dimensional and 3D images of the white matter tracts and create 3D models and augmented and virtual reality simulations.
METHODS: Twenty cadaveric brain specimens were prepared in accordance with the Klingler method. Brain hemispheres were dissected step-by-step from lateral-to-medial and medial-to-lateral directions. Three-dimensional models and augmented reality and virtual reality simulations were built with photogrammetry.
RESULTS: High-resolution 3D models and augmented reality and virtual reality simulations of the white matter anatomy of the cerebrum were obtained. These models can be freely shifted and rotated on different planes, projected on any real surface, visualized from both front and back, and viewed from various angles at various magnifications.
CONCLUSION: To our knowledge, this is the first detailed study integrating various technologies (3D modeling, augmented reality, and virtual reality) for high-resolution 3D visualization of dissected white matter fibers of the entire human cerebrum.
Performing safe and successful surgery on cerebrum lesions requires a good understanding of the 3-dimensional (3D) topographic anatomy of the cerebral fiber tracts in the human brain and their interrelationships. White matter tracts have long been an essential component of neuroanatomy and neurosurgery education. The fiber dissection technique was used and developed by early anatomists such as Raymond Vieussens (1641–1715), Johann Christian Reil (1759–1813), Achille-Louis Foville (1799–1878), and Friedrich Arnold (1803–1890).1 In the 20th century, Joseph Klingler made the biggest breakthrough in this regard and added the freezing technique.1-3 In the 1990s, the senior author (UT) developed a strong interest in this field and revitalized the fiber dissection technique, and with the invention of DTI tractography through this method, the fiber dissection technique was accepted worldwide.1
White matter fiber dissection is an important method for acquiring a detailed understanding of neuroanatomical structures in preparation for surgical practice. Previous research has aided our understanding of brain anatomy and highlighted the importance of this technique in modern neurosurgery.1,4-11 However, as obtaining cadaveric materials requires financial and ethical considerations, cadaver-based neuroanatomy training is not available in all neurosurgery institutions around the world. Furthermore, there is currently no 3D model or augmented reality (AR) or virtual reality (VR) simulation guide in the literature for the dissection of white matter tracts. Neuroanatomical models have proven useful in diagnosis, surgical planning, and training in neuroscience and medicine.12-15 New approaches that emphasize 3D anatomical relationships using imaging techniques are currently displacing traditional techniques.16-20
Photogrammetry is a technique for creating interactive, realistic digital models of cadaveric specimens by overlapping 2-dimensional (2D) images to create digital 3D models.21 VR is a cutting edge human-computer interface that creates a realistic world.22 This virtual world allows participants to move around freely. They can look at the model from various perspectives and reach into it. AR refers to a real-time direct or indirect view of a physical real-world environment that has been enhanced or augmented by the addition of virtual computer-generated information. While VR technology fully immerses users in a virtual environment without allowing them to see the actual world, AR technology enhances the sense of reality by superimposing virtual objects and cues onto the real world in real time.22
As a result, our main goal is to provide detailed, step-by-step 3D models and AR and VR simulations of cerebral white matter dissection, highlighting sequential dissection stages and critical technical nuances that aid this difficult technique. These high-fidelity and accessible 3D models and AR and VR simulation of the dissection of cerebral white matter tracts can enhance the training of neurosurgeons, anatomists, and medical students worldwide.
According to the policy of the institution where this research was conducted, ethics committee approval is not mandatory for this kind of study.
We used 20 adult cadaveric cerebral hemispheres (10% formalin-fixed) for this study in the Yeditepe University Microsurgery-Neuroanatomy Laboratory. The specimens were frozen for at least 2 weeks at −15 degrees celsius and thawed under water for 1 hour.
With the help of a microsurgical set (Rhoton dissector, wooden spatula, dissector, and forceps), the specimens were dissected under the operating microscope (Carl Zeiss Opmi 1 SH Surgical Microscope Contraves; x6, x10, x25 magnification) in stepwise fashion from the lateral-to-medial and medial-to-lateral surfaces with the fiber dissection technique. To prepare 3D anaglyph images, each stage of the dissection was photographed in 3D. Each 3D image was positioned next to or above a labeled 2D image. Adobe Photoshop CC was used to create the anaglyph images, which are viewed with red and blue glasses (Adobe).
As mentioned in our previous study, each stage of dissection was captured with a photogrammetry application (Qlone, 2017-2020 EyeCue Vision Technologies, Ltd.) to create 3D models and AR and VR simulations.23 Briefly, 2D images of specimens are taken at various angles and then overlaid using the application to create a 3D reconstruction of photogrammetry. As a result, this model displays both geometric and textural information from the real specimen. The obj, stl, fbx, usd, glb, x3D, ply formats of the 3D models and AR and VR simulations of the dissected specimens were created. These models and simulations are freely available on The Neurosurgical Atlas website.24 These files can be opened on Apple devices without additional applications, and the models can be viewed in any 3D, AR viewing program (Qlone, Sketchfab, Emb3D, 3D Viewer etc.) on Android or Microsoft devices (Figure 1A). The models can be moved and rotated in all directions. Because of the AR compatibility, the model can be projected on any real surface, and the specimens can be viewed from both front and back (Figure 1B). In this way, it can be projected next to the surgeon’s own specimen during dissection for comparison.
Anatomical dissection begins with a detailed inspection of the essential sulci and gyri on each hemispheric surface along with the arachnoid membrane and vessels (Figure 2A and 2B, Video 1). The arachnoid membrane and vessels are then removed (Figure 2C and 2D, Video 1), revealing the U fibers (Figure 2E and 2F, Video 1). After the U fibers are removed, the arcuate fasciculus becomes visible. This structure is a superficial long-connection fiber pathway, which connects Broca and Wernicke areas, the language centers (Figure 3A and 3B, Video 1).25 The major component of superior longitudinal fasciculus (SLF) is SLF II, which starts in the caudal-inferior parietal cortex and ends in the dorsolateral prefrontal cortex. SLF III is the ventral component and terminates in the ventral premotor and prefrontal cortex (Figure 3A and 3B, Video 1).
The central core of the cerebrum is located between the insular cortex laterally and the ventricles medially.4 The insula has an irregular, triangular shape (Figure 3C and 3D, Video 1)26 and becomes visible when the operculum is removed. The lateral surface of the insula is divided into anterior and posterior portions by the central sulcus of insula, which is located between the short and long gyri (Figure 3C-H, Video 1). U fibers between the adjacent insular and opercular gyri are visible when the insular cortex is removed. These fibers are defined as the superficial layer of the extreme capsule (Figure 3E-H, Video 1). The uncinate fasciculus and fronto-occipital fasciculus are exposed when the U fibers (the superficial layer of the extreme capsule) at the level of the limen insula are removed (Figure 3I and 3J, Video 1). The fronto-orbital cortex and the temporopolar cortex are connected by the uncinate fasciculus. The fronto-occipital fasciculus is a long association fiber in the dorsomedial uncinate fasciculus. The frontal cortex is connected to the occipital, temporal, and parietal cortices by fronto-occipital fasciculus fibers. The claustrocortical fibers, which are a component of the external capsule, are visible after the U fibers have been removed (Figure 3I and 3J, Video 1). Claustrocortical fibers are fibers that originate from the claustrum and go to higher cortical areas. The putamen, a well-defined gray matter mass that appears when the external capsule and claustrum are taken out, is removed with an aspiration system or dissector (Figure 3K-P, Video 1). When the putamen is partially removed, the globus pallidus is exposed (Figure 3Q-T, Video 1). Removing the globus pallidus exposes the anterior commissure and internal capsule (Figure 3U-X, Video 1).27
The inferior longitudinal fasciculus is located below the axial level of the inferior temporal gyrus (Figure 3M and 3N, Video 1). When the fronto-occipital and inferior longitudinal fasciculi are removed, the optic radiation is revealed (Figure 3W and 3X, Video 1). The sagittal stratum is a polygonal crossroads of associational fibers situated deep on the lateral surface of the hemisphere, medial to the arcuate fascicle complex and lateral to the tapetum fibers of the atrium (Figure 3W and 3X, Video 1).28
The medial side of the hemisphere was photographed before the medial surface dissection was begun (Figure 4A and 4B, Video 2). The arachnoid membrane and vessels are removed (Figure 4C and 4D, Video 2). Then, the cortex is removed (Figure 4E and 4F). The cingulate gyrus is visualized (Figure 4G and 4H, Video 2).29 Removing the cingulum exposes the corpus callosum (Figure 4I and 4J, Video 2).
The ventricular ependyma is gently peeled from the frontal horn, and the lateral ventricle body after the corpus callosum is resected. As a result, the head and body of the caudate nucleus are exposed (Figure 4K and 4L, Video 2).
The inferior fibers of the cingulum are removed, and the temporal horn of the lateral ventricle and the hippocampus are visualized. The hippocampus is located in the floor of the temporal horn, the anterior section of the atrium, and inferomedial to the temporal lobe gyrus (Figure 4M and 4N, Video 2).30,31
The anatomical relationship between the fornix and thalamus was then documented (Figure 4M and 4N, Video 2).32 The stria medullaris thalami, which extends from the habenular area to the septohypothalamic zone, and the fornix are two white-matter fasciculi that cross the superior surface of the thalamus (Figure 4M and 4N, Video 2). The fornix and caudate nucleus are removed, and the thalamic fibers are exposed (Figure 4O and 4P, Video 2).
As cadaveric-based research declines, neurosurgeons have been encouraged to conceptualize complex 3D anatomy and spatial relationships from 2D images found in standard textbooks.33 The traditional tools used to teach anatomy are 2D anatomic atlases, lectures, and courses in cadaveric dissection. Although schematic drawings and diagrams are often used to illustrate brain anatomy, spatial comprehension is a complex mental process that requires one to imagine a 3D structure based on a 2D picture. However, because of impediments such as a lack of cadavers, dissection courses have been reduced. Although physical cadavers are available in only some places, neurosurgeons can use digital learning resources at any time and from any place. Daily access to anatomical variety that could be difficult to find in the laboratory can be provided by digital libraries of anatomical specimens.
White matter tracts are important in determining the margins of resection during surgery because they provide cerebral connections. Therefore, it is very important to understand the 3D anatomy of the white matter pathways. Furthermore, understanding and interpreting 3D anatomical relationships are important for clinical practice and neurosurgical operations, with the use of advanced imaging and the transition to minimally invasive surgery.7,8 The fiber dissection technique is one of the techniques that allows us to understand the 3D relationships of these structures. Klingler and colleagues developed the Klingler process, an improved method of brain fixation.3,34 This anatomic research serves as a comprehensive 3D modeling and AR and VR simulation dissection manual for those studying cerebral anatomy. This technology creates a fully immersive and interactive experience and is being used at all levels of medical education, and its popularity is expected to increase.35 Photogrammetric 3D models and AR and VR simulations attract attention in neuroanatomy education.36 As compared with other acquisition methods (CT, MRI, or laser scans), 3D modeling with 360-degree photogrammetry is a relatively easy and inexpensive option for daily practice.21 Another advantage is that, once developed, these high-quality 3D models can be freely transferred and shared electronically. Furthermore, cadaveric specimens can be stored in digital format, which eliminates the problems of decay and discoloration that occur over time. These 360-degree models can also be printed in 3D,37 which may thus be used to replace or supplement human cadavers.
The availability of digital 3D anatomical models is particularly notable. As compared with 2D images, 3D models and AR and VR simulation add an extra dimension that improves the quality of visual information as well as the usefulness of surface visualization in neurosurgery. Furthermore, it has been demonstrated that guided 3D manipulation of anatomical specimens improves neurosurgeons' success in certain spatial capacity and structural recognition tasks. Neurosurgeons also realize the benefit of digital 3D models in visualizing some aspects of neuroanatomy. As these developments continue, incorporating AR and VR into anatomy education should become easier.38 These teaching tools have been shown to increase performance in neuroanatomy education and have become a complementary part of neurosurgical education.39
Previous research has focused on the anatomical characteristics of the fiber tracts of the cerebrum.1,4 These studies have improved our understanding of cerebral white matter and fiber tract anatomy, but they are scattered in the neurosurgical literature and do not provide the reader with a detailed, step-by-step 3D model or AR and VR simulations for the entire dissection process. Most articles have focused on 2D images, which lack a sense of the depth necessary for accurate comprehension of the complex anatomy of white matter tracts. Rhoton and associates published the Rhoton collection,40 and Cohen-Gadol and colleagues published The Neurosurgical Atlas,24 both of which greatly contributed to neurosurgery education. Our aim was to combine these two approaches to create incremental models in real cadavers. Our future goal is to create 3D segmental dynamic cadaveric models.
This is the first 3D model with augmented and virtual reality simulation that serves as a manual for this topic, orienting neurosurgeons by making the entire procedure simple. The aim of this study was to explain the procedures for the fiber dissection technique, create 3D models and AR and VR simulations, and make complex white matter anatomy more understandable. We believe that systematic studies using 3D models and AR and VR simulations of the fiber dissection technique have the potential to uncover a bank of knowledge that will aid our understanding of microneurosurgery, the development of our techniques, and anatomic and radiological knowledge of the fiber tracts, and improve surgical planning and strategy.
A better understanding of the 3D anatomical organization of the fiber pathways is needed to plan safe and successful surgery for lesions in the cerebrum. Therefore, the current study presents a 3D model with AR and VR simulation of the cerebral white matter tracts. This study is a free, high-fidelity digital library of 3D cadaver models available to anyone interested in cerebral white matter anatomy. This resource has the potential to change neuroanatomy education.
Contributors: M. E. Gurses, A. Gungor, E. Gökalp, S. Hanalioglu, S. Y. K. Okumus, I. Tatar, M. Berker, A. A. Cohen-Gadol, and U. Türe
Content from Gurses ME, Gungor A, Gökalp E, Hanalioglu S, Okumus SYK, Tatar I, Berker M, Cohen-Gadol AA, Türe U. Three-dimensional modeling and augmented and virtual reality simulations of the white matter anatomy of the cerebrum. Oper Neurosurg (Hagerstown) 2022;23:355-366. doi.org/10.1227/ons.0000000000000361. With permission of Oxford University Press on behalf of the Congress of Neurological Surgeons. © Congress of Neurological Surgeons.
- Ture U, Yasargil MG, Friedman AH, et al. Fiber dissection technique: lateral aspect of the brain. Neurosurgery 2000;47:417-426; discussion 426-427.
- Silva SM, Andrade JP. Neuroanatomy: the added value of the Klingler method. Ann Anat 2016;208:187-193.
- Agrawal A, Kapfhammer JP, Kress A, et al. Josef Klingler's models of white matter tracts: influences on neuroanatomy, neurosurgery, and neuroimaging. Neurosurgery 2011;69:238-252; discussion 52-54.
- Ture U, Yasargil DC, Al-Mefty O, et al. Topographic anatomy of the insular region. J Neurosurg 1999;90:720-733.
- Kucukyuruk B, Yagmurlu K, Tanriover N, et al. Microsurgical anatomy of the white matter tracts in hemispherotomy. Neurosurgery 2014;10 Suppl 2:305-324; discussion 324.
- Ribas EC, Yagmurlu K, Wen HT, et al. Microsurgical anatomy of the inferior limiting insular sulcus and the temporal stem. J Neurosurg 2015;122:1263-1273.
- Yagmurlu K, Vlasak AL, Rhoton AL, Jr. Three-dimensional topographic fiber tract anatomy of the cerebrum. Neurosurgery 2015;11 Suppl 2:274-305.
- Gungor A, Baydin S, Middlebrooks EH, et al. The white matter tracts of the cerebrum in ventricular surgery and hydrocephalus. J Neurosurg 2017;126:945-971.
- Ribas EC, Yagmurlu K, de Oliveira E, et al. Microsurgical anatomy of the central core of the brain. J Neurosurg 2018;129:752-769.
- Parraga RG, Possatti LL, Alves RV, et al. Microsurgical anatomy and internal architecture of the brainstem in 3D images: surgical considerations. J Neurosurg 2016;124:1377-1395.
- Serra C, Ture U, Krayenbuhl N, et al. Topographic classification of the thalamus surfaces related to microneurosurgery: a white matter fiber microdissection study. World Neurosurg 2017;97:438-452.
- Johnson EO, Charchanti AV, Troupis TG. Modernization of an anatomy class: from conceptualization to implementation. A case for integrated multimodal-multidisciplinary teaching. Anat Sci Educ 2012;5:354-366.
- Meakin JR, Shepherd DE, Hukins DW. Short communication: fused deposition models from CT scans. Br J Radiol 2004;77:504-507.
- Muller A, Krishnan KG, Uhl E, et al. The application of rapid prototyping techniques in cranial reconstruction and preoperative planning in neurosurgery. J Craniofac Surg 2003;14:899-914.
- Harput MV, Gonzalez-Lopez P, Ture U. Three-dimensional reconstruction of the topographical cerebral surface anatomy for presurgical planning with free OsiriX software. Neurosurgery 2014;10 Suppl 3:426-435; discussion 435.
- Kelley DJ, Farhoud M, Meyerand ME, et al. Creating physical 3D stereolithograph models of brain and skull. PLoS One 2007;2:e1119.
- Fernandez-Miranda JC, Rhoton AL, Jr., Alvarez-Linera J, et al. Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery. 2008;62(6 Suppl 3):989-1026; discussion 1028.
- Lukic IK, Gluncic V, Ivkic G, et al. Virtual dissection: a lesson from the 18th century. Lancet 2003;362:2110-2113.
- Chen JC, Amar AP, Levy ML, et al. The development of anatomic art and sciences: the ceroplastica anatomic models of La Specola. Neurosurgery 1999;45:883-891; discussion 891-892.
- Akbaş A, Tuğcu B, Ekşi MŞ, et al. Robotic surgical approach to the mesial temporal region: a preliminary three-dimensional cadaveric study of technical feasibility. World Neurosurg 2020;144:e40-e52.
- Petriceks AH, Peterson AS, Angeles M, et al. Photogrammetry of human specimens: an innovation in anatomy education. J Med Educ Curric Dev 2018;5:2382120518799356.
- Huang KT, Ball C, Francis J, et al. Augmented versus virtual reality in education: an exploratory study examining science knowledge retention when using augmented reality/virtual reality mobile applications. Cyberpsychol Behav Soc Netw 2019;22:105-110.
- Gurses ME, Gungor A, Hanalioglu S, et al. Qlone®: a simple method to create 360-degree photogrammetry-based 3-dimensional model of cadaveric specimens. Oper Neurosurg (Hagerstown) 2021;21(6):E488-93.
- The Neurosurgical Atlas, https://www.neurosurgicalatlas.com/. Accessed Web. 30 January 2022.
- Martino J, Hamer PC, Berger MS, et al. Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 2013;218(1):105-21.
- Uddin LQ, Nomi JS, Hebert-Seropian B, Ghaziri J, Boucher O. Structure and Function of the Human Insula. J Clin Neurophysiol 2017;34(4):300-6.
- Peltier J, Verclytte S, Delmaire C, et al. Microsurgical anatomy of the anterior commissure: correlations with diffusion tensor imaging fiber tracking and clinical relevance. Neurosurgery 2011;69(2 Suppl Operative):ons241-246; discussion ons246-247.
- Di Carlo DT, Benedetto N, Duffau H, et al. Microsurgical anatomy of the sagittal stratum. Acta Neurochir 2019;161:2319-2327.
- Bubb EJ, Metzler-Baddeley C, Aggleton JP. The cingulum bundle: anatomy, function, and dysfunction. Neurosci Biobehav Rev 2018;92:104-27.
- Teyler TJ, DiScenna P. The topological anatomy of the hippocampus: a clue to its function. Brain Res Bull 1984;12:711-719.
- Giap BT, Jong CN, Ricker JH, et al. The hippocampus: anatomy, pathophysiology, and regenerative capacity. J Head Trauma Rehabil 2000;15:875-894.
- Ozer MA, Kayalioglu G, Erturk M. Topographic anatomy of the fornix as a guide for the transcallosal-interforniceal approach with a special emphasis on sex differences. Neurol Med Chir (Tokyo) 2005;45:607-612; dsicussion 612-613.
- Estevez ME, Lindgren KA, Bergethon PR. A novel three-dimensional tool for teaching human neuroanatomy. Anat Sci Educ 2010;3:309-317.
- Wysiadecki G, Clarke E, Polguj M, et al. Klingler's method of brain dissection: review of the technique including its usefulness in practical neuroanatomy teaching, neurosurgery and neuroimaging. Folia Morphol (Warsz) 2019;78:455-466.
- Drake RL, McBride JM, Lachman N, et al. Medical education in the anatomical sciences: the winds of change continue to blow. Anat Sci Educ 2009;2:253-259.
- Kockro RA, Amaxopoulou C, Killeen T, et al. Stereoscopic neuroanatomy lectures using a three-dimensional virtual reality environment. Ann Anat 2015;201:91-98.
- McMenamin PG, Quayle MR, McHenry CR, et al. The production of anatomical teaching resources using three-dimensional (3D) printing technology. Anat Sci Educ 2014;7:479-486.
- Riva G, Wiederhold BK. The new dawn of virtual reality in health care: medical simulation and experiential interface. Stud Health Technol Inform 2015;219:3-6.
- Rizzolo LJ, Rando WC, O'Brien MK, et al. Design, implementation, and evaluation of an innovative anatomy course. Anat Sci Educ 2010;3:109-120.
- The Rhoton Collection, http://rhoton.ineurodb.org/mobile. Accessed Web. March 10, 2021.
Please login to post a comment.