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Stereoscopy in Surgical Neuroanatomy: Past, Present, and Future

Roberto Rodriguez Rubio, Since the of antiquity, scientists, philosophers, and artists have pondered the nature MD ‡§¶∗ of optical —the perception of depth that arises from . The Rina Di Bonaventura, MD§∗ early19thcenturysawtheadventofstereoscopes,devicesthatcouldreplicatestere-

Ioannis Kournoutas, BS§ opsis by producing a 3D illusion from the super-imposition of 2D . This Downloaded from https://academic.oup.com/ons/article/18/2/105/5520488 by guest on 26 September 2021 phenomenon opened up a plethora of possibilities through its usefulness as an educa- Dania Barakat, BA§ tional tool—particularly in medicine. Before long, photographers, anatomists, and physi- § Vera Vigo, MD cians were collaborating to create some of the first stereoscopic atlases available for the Ivan El-Sayed, MD§¶ teaching of medical students and residents. In fields like neurosurgery—where a compre- Adib A. Abla, MD‡§ hensive visuospatial understanding of neuro-anatomical correlates is crucial—research into stereoscopic modalities are of fundamental importance. Already, medical institutions ‡ Department of Neurological Surgery, all over the world are capitalizing on new and immersive technologies—such as 3D intra- University of California, San Francisco, California; §Skull Base and Cerebrovas- operative recording, and 3D endoscopes—to refine their pedagogical efforts as wellas cular Laboratory, University of California, improve their clinical capacities. The present paper surveys the history of stereoscopy ¶ San Francisco, California; Department of from antiquity to the modern era—with a focus on its role in neurosurgery and medical Otolaryngology - Head and Neck Surgery, University of California, San Francisco, education. Through the tracking of this evolution, we can discuss potential benefits, future California directions, and highlight areas in which further research is needed. By anticipating these factors, we may strive to take full advantage of an emergent field of technology, for our ∗These authors contributed equally to this work. ultimate goal of improving patient care. KEY WORDS: Three-dimensional, History, , Neuroanatomy, Education, 3D , 3D , Correspondence: Volumetric models, Extended reality, , Holograms Roberto Rodriguez Rubio, MD, Department of Neurosurgery and OHNS, Operative Neurosurgery 18:105–117, 2020 DOI: 10.1093/ons/opz123 Skull Base & Cerebrovascular Laboratory, University of California, San Francisco, 513 Parnassus Ave HSE 817 Box 0112, San Francisco, CA 94143. euroanatomy—the study of the organi- Stereopsis—the perception of depth that Email: [email protected] zation of the central nervous system— results from binocular vision—has long been N is one of the most fascinating and investigated as a feature to be manipulated Received, October 11, 2018. ancient topics within anatomy. Historically, its for educational and functional ends. Research Accepted, December 13, 2018. Published Online, June 19, 2019. teaching in the medical context has been rooted into SS modalities has yielded many notable in cadaveric dissections and dates back to the products that can emphasize the spatial corre- C Congress of Neurological Surgeons ancient Greek physician Herophilos (335-280 lations between neurovascular structures. Some 2019. BC). Through the ages, the primary challenge of of these recent technological advancements in This is an Open Access article distributed neuroanatomy has been in learning the intricate neurosurgery include: 3D systems under the terms of the Creative 3-dimensional topography—an oft difficult task for surgical microscopes, 3D endoscopes, 3D Commons Attribution- given the scarcity of cadaveric specimens and exoscopes, virtual reality (VR) simulators, NonCommercial-NoDerivs licence 1 (http://creativecommons.org/licenses/ the 2D nature of drawings and photographs. surgical robotics, and advanced neuroimaging by-nc-nd/4.0/), which permits In the context of , anatomists refer to apparatuses. non-commercial reproduction and 3D images and 3D videos as “stereoscopic” Tracking the history of this transition from distribution of the work, in any medium, (SS)—nomenclature based on the phenomena of 2D representation to 3D imaging allows us to provided the original work is not altered or transformed in any way, and that the stereopsis. speculate on future directions. This paper offers work is properly cited. For commercial a historical narrative on stereoscopy—including re-use, please contact its first applications in neuroanatomy and neuro- [email protected] ABBREVIATIONS: SS, Stereoscopy; VM, Volumetric surgery, with the goal of highlighting its unique models; VR, virtual reality value in medical pedagogy.

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THE ORIGINS OF STEREOSCOPY

The fundamentals of stereoscopy are based on the fact that humans have a binocular vision—a feature that allows for . As early as 300 BC, Euclid observed that an image of an object seen by a person’s 2 eyes was dissimilar2—the disparity between the left and right eye allowed for 2 unique viewing angles. Later Ptolemy (AD 127-165), expanded and formalized Euclid’s ideas in his 5-volume work “Optica”.3 Soon after, Galen (ca. AD 129-201) also described this phenomenon—dubbed binocular —in which each eye sees distinct parts of an object which are then perceived as a unified 3D image. Downloaded from https://academic.oup.com/ons/article/18/2/105/5520488 by guest on 26 September 2021 During the medieval dark ages in Europe, Middle-Eastern scholars such as Ibn al-Haytham (965-1040AD) continued to study the physiology of —his magnum opus, the “Book of Optics” promoted the theory that perception arises from light entering the eye at different angles.4 Centuries later Leonardo da Vinci (1452-1519), noted that “certain portions of distant objects that were hidden from one eye by a near object became visible to the other eye when it was opened”.5 On several occasions Da Vinci expressed his frustration that a 2D painting could never fully recreate the depth experienced when viewing FIGURE 1. A lenticular stereoscope. Public Domain. real objects.6,7 While many more scientists documented this phenomenon of binocular disparity and its role in perception, it was not until the 19th century that the principle of stereoscopy began to flourish. Nevertheless, SS modalities continued to evolve was fully elucidated and techniques to reproduce stereopsis were 8 developed.8,9 as their scientific applications remained useful. In 1832, Sir (1802-1875) demonstrated that it was possible to artificially reproduce 3D-binocular vision FROM THE STEREOSCOPE TO THE by super-imposing slightly different drawings of an object VIEWMASTER: NEUROANATOMICAL through optical means.10,11 He invented the first stereoscope and APPLICATIONS utilized different types of prisms and mirrors to customize the SS effect. In June 1838, his discovery was formally published and Among the earliest users of the newly evolved - presented before the Royal Society of London. The advent of early in the scientific realm were medical scholars who photographic techniques led Wheatstone, early in 1839, to reach taught their interns through three-dimensional imaging of human out to Fox Talbot to prepare SS talbotypes of statues, buildings, anatomy. and even portraits.12 Ten years later, British scientist Sir David The first collection of anatomic SS illustrations was prepared by Brewster made SS pictures via the newly minted Scottish anatomist Daniel John Cunningham (1850-1909). His process, the first commercially successful photographic method, work “Stereoscopic Studies of Anatomy” was published in 1905 and which was invented by Louis-Jacques-Mandé Daguerre. was composed of 5 sections among which 1 cataloged the central In 1844, Brewster went on to invent an improved stereoscope, nervous system (Figure 2). Later, in 1919, after Cunningham’s the “lenticular stereoscope”, which was the first portable, 3D death, the collection was edited by a former collaborator named viewing device (Figure 1). It employed prismatic lenses made David Waterston, who organized a new 10 Volume work with from a double convex lens cut across its diameter—which he 324 SS photographs.15 This collection repre- put in place of the mirrors and prisms employed by Wheat- sents a remarkable set of original SS photographs, each of which stone. With this stereoscope, Brewster was able to view a 3D is mounted on a card stock and designed to be viewed through a image created by the superimposition of 2 individual photographs SS viewer. taken by a which was moved sideways, by a distance of A similar collection—but one totally focused on 2.5” between the 2 exposures13—to mimic binocular disparity. SS neuroanatomy—was produced in 1947 by H. S. Rubinstein became commercially available around 1857 and interest and C.L. Davis. Their atlas of neuroanatomy was published by in stereoscopy began to rise exponentially. At one point, enthu- Grune & Stratton, New York,16 and offered 43 plates printed on siasts formally founded a Stereoscopic Society, an organization heavy cardboard and an accompanying descriptive manual. The with the slogan “no home without a stereoscope”.14 Overtime, the plates portrayed the SS photographs of cortical specimens, while allure of SS photography gradually declined as the industry the manual outlined the methodology behind the dissections.

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FIGURE 2. Title page of the first stereoscopic book published in 1905: “Stereoscopic Studies of Anatomy” by Daniel John Cunningham. Public Domain.

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However, the largest and most notable SS project for pedagogy took over 10 yr to finish. The final set was edited to 221 reels was developed in the United States after a successful meeting with 1547 SS images depicting the hundreds of soft tissue dissec- between the German photographer Wilhelm Gruber (1903- tions performed by Bassett for his Stanford University courses.18 1965) and the American anatomist David Lee Bassett (1913- With its portable form, accessibility, and ease-of-use, this work 1966). Gruber had moved to the USA during his twenties, and his aimed to serve not only as an atlas but as a guide for dissections. passion for photography had led him to invent the ViewMaster Basset wrote: “Each exploratory sequence is permanently recorded by (Mattel Inc, El Segundo, California), a portable and affordable means of stereoscopic photography on transparency . This SS viewer which was presented for the first time at the World’s 3D technique brings to the viewer every illusive detail, every tone Fair in New York in 1939.17 This device operated by loading a and color, every topographical relation exactly as it was seen by the pre-set reel of SS images, which the user could switch between. dissector”.19 It quickly became popular, and the United States military even commissioned the production of millions of sets of reels to aid THE EVOLUTION OF SS PHOTOGRAPHY IN Downloaded from https://academic.oup.com/ons/article/18/2/105/5520488 by guest on 26 September 2021 with artillery spotting and aircraft identification during World NEUROSURGERY War II.17 By 1947, the success of the ViewMaster was solid- ified, and the partnership between Gruber and Bassett gave rise Following the aforementioned landmark project, which is to the project titled “Stereoscopic Atlas of Human Anatomy”, which considered a milestone in 3D anatomical representation, many

FIGURE 3. A, Front cover of the first stereoscopic surgical atlas: “The Stereoscopic Atlas of Mastoidotympanoplastic Surgery”, B, Interior: Stereoscopic reels, segmented in a stepwise fashion according to the procedure. C Elsevier, used with permission.

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FIGURE 3. Continued.

other developments followed suit. “The Stereoscopic Atlas of of the atlas, the authors highlight that “becoming familiar and Mastoidotympanoplastic Surgery”(Figure3AandB)byHarold comfortable with 3D geometry of neurosurgical anatomy is often F. Schuknecht, Werner D. Chasin and John M. Kurkjian,20 the most difficult and the last aspect of one’s training, frequently is a photographic atlas published in 1966 by the C.V. Mosby being achieved long after the development of the fine microsurgical Company. Its declared aims are to show the important histopatho- technique”.21 logic changes in chronic suppurative middle ear and mastoid Another work dedicated to resident education was “The Micro- disease and to describe the surgical procedure. This work repre- surgical Anatomy of the Brain—A Stereoatlas”byGaryE.Kraus sents the first application of stereoscopy beyond merely educating and Gregory J. Bailey, published by Waverly Europe Ltd, London, medical students; residents could now benefit from 3D represen- in 1994.22 This atlas cataloged various routes for approaching tations of surgical techniques. intracranial lesions and consisted of stereophotographs taken In 1985, the Mosby Company published another SS work, from dissections performed at the Barrow Neurological Institute “The Stereoatlas of Operative Microneurosurgery”(Figures4A-C) by in Phoenix, Arizona. Charles E. Poletti and Robert G. Ojemann.21 This work, designed These 3 landmark applications of stereoscopy in neuro- for neurosurgical residents, included 24 View-Master reels with surgery were inspirational for many neurosurgeons, including the 168 stereo color slides taken through the operating microscope renowned Albert J. Rhoton, professor at University of Florida, during neurosurgical procedures. The slides not only accurately whose laboratory pioneered many microneurosurgical concepts depicted the intraoperative 3D anatomical visuospatial relation- and techniques.23 For more than 40 yr, Dr Rhoton produced ships, but also allowed viewers to perceive features such as texture, valuable tools for educating neurosurgeons all over the world, color, shape, delineation, and degree of lucency. In the preface and his legacy has contributed to improving the reliability and

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FIGURE 4. A, Front cover of “The Stereoatlas of Operative Microneurosurgery”. B, Instructional demonstration. C,Interior: Accompanying reels. C Elsevier, used with permission.

safety of neurosurgical approaches already in use.24-29 Recog- remain an affordable method at achieving a 3D effect. Subse- nizing their potential, Dr Rhoton embraced the advantages of quent developments include prismatic lenses, polarized (passive) teaching neuroanatomy with SS photographs in 1999, which he , (active) glasses, (Google LLC, would use to supplement his papers and lectures.30-33 Mountain View, California), and VR displays (Figure 5).35 During this period, due to the increasing interest in stere- oscopy, new visualizing systems were also being developed. The Stereoscopy and Neurosurgery: Current most significant development came with the transition from Today, a developing field in SS neuroanatomy is the 3D the stereoscope viewer to anaglyph glasses which produced a recording of neurosurgical operations.36-39 Just as standard 2D 3D image through anaglyph color filtering—a method based videos evolved from 2D images, so are 3D videos slowly but surely on Wilhelm Rollmann’s studies in 1853.34 These were the first evolving from the kind of static SS images previously described. 3D mobile glasses used for SS neuroanatomy/neurosurgery and An increasing number of programs have become aware that SS

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FIGURE 4. Continued.

imaging contributes to the acceleration of the learning curves of technology, the complexity of the capture techniques, perceived trainees by providing them a more detailed appreciation of the discomfort in using 3D glasses, and skepticism regarding surgical anatomy.40-45 The potential benefits of the SS displays are its effectiveness. In recent years, several studies have been many, including enhanced image quality, easier discrimination of conducted to compare the efficacy of 3D vs 2D in neuro- the structure of interest from surrounding tissues, and improved surgical education. While many have found SS lectures to be surface detection/depth judgment—all factors that are critical beneficial in teaching,48,49 some have suggested that the effect during the intraoperative decision-making process. Therefore, a is not significant.50 The main limitations of most 3D studies 3D display of a microneurosurgery represents a precious resource are the subjective assessments, which mostly rely on self-reported for observers in the operating rooms and residents in training.46 measures. In addition, no studies have assessed the acquisition and Furthermore, recorded 3D videos provide an excellent oppor- long-term retention of information learned through SS modal- tunity for education, as anatomical relationships can be easily ities. Due to these factors, both the development of objective reviewed and used in lectures and publications. They are quickly assessment methods—as well as longitudinal study designs—will becoming part of cutting-edge operating rooms all around the be crucial in further elucidating the efficacy of stereoscopy in the world.47 academic context. Since 2010, there has been a significant increase in the publi- cation rate of SS video articles on peer-reviewed neurosurgical FUTURE DIRECTIONS journals. Nevertheless, many neurosurgeons around the world have not entirely embraced SS technologies. Reasons for this Neurosurgery itself could be described as a 4-D process include the cost of equipment: time spent troubleshooting the that requires the operator to move through time in a 3D

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FIGURE 4. Continued.

anatomical space. Much like a sculptor or a 3D artist, SS videos, the latest frontier includes the development of the surgeon must manipulate dynamic and ever-changing 3D or volumetric models (VM) that can be interacted with variables in a real time—a skill that requires extensive practice. for educational and surgical planning purposes. Whereas a Whereas cadaveric dissections and intraoperative surgery are standard SS photo is an created with two crucial exercises, limitations in opportunity for using these photos, VM reconstructions operate within a Cartesian plane— tools highlight the need for new and improved alterna- a feature that makes them particularly useful in developing 3D tives. Beyond the traditional 3D anatomical pictures and technologies.

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FIGURE 5. Snapshot of the evolution of modern stereoscopic viewers, pictured (left to right): anaglyph glasses, prismatic lenses, polarized (passive) glasses, shutter (active) glasses, Google Cardboard, virtual-reality headset.

This is a trend that began almost 20 yr ago, as educators started 2013, and 201470-72 reviewed their experience of predissection to investigate 3D ,51-53 simulators,54-56 and and postdissection DICOM images of specimens, performing computer animations.57,58 Despite high costs of production, this CT scans before and after the dissections to create geometric technology has been widely recognized for its value in medical models of the approach in their laboratory. However, VM models education and has been quickly deployed in neuroanatomy.59 The created from DICOM (e.g, computed tomography, magnetic origins of 3D anatomical models can be traced to the Visible resonance imaging) or rendering software offer limited textural Human Project, conceived in 1988 by the National Library features. For this reason, some research teams working on the of Medicine (NLM), the world’s largest biomedical library on creation of a volumetric depiction of surgical neuroanatomy the campus of the National Institutes of Health in Bethesda, have collaborated with 3D artists, who can optimize the Maryland.60-62 It had been designed to serve as the first VM graphical features of these models for their use in neurosurgical anatomical data set, and as a cornerstone for future sets of related education.73,74 image libraries. The first atlas—part of the Visible Human Male There are a number of recent technologies that can overcome study—consisted of a collection of 1878 one-millimeter thick some of the limitations inherent in DICOM samples—including transverse slices obtained with a cryomacrotome from a previously photography (stereophotogrammetry) or scanning.75-77 VM preserved body of a male donor. Anatomical axial, sagittal, and models derived through these techniques are in many ways coronal reconstructions were synthesized to create 3D reconstruc- superior to traditional SS photography. VM models allow the tions of the entire body. The Visible Human Male and subsequent exploration of dissected structures not only in standard 2D projects led to the development of many other projects in human but in a 360◦SS view of the object. Surface recon- anatomy that also produced relevant contributions to anatomical struction through techniques provides excellent research and education.63-66 This methodology was directly color and texture feedback, which more accurately replicate the applied to neurosurgery in 2011 when Liu et al67 described the surgical anatomy emphasized by the dissector. The interactive computerized freezing milling technique used to obtain a 3D experience of neuroanatomy and neurosurgery that 3D modeling reconstruction of the sellar region from thin coronal sections of can offer is enhanced through its encounter with 3D platforms— a cadaveric specimen. This work aimed to help surgeons under- the most popular being VR.78 stand anatomical nuances based on relevant neuroanatomy. VM VR is a form of extended reality, defined as the combined built from DICOM (digital imaging and communications in total of human-machine interactions generated by technology medicine) have represented yet another evolution for imaging and wearables.79 The advent of this modality came in 1968 and have seen applications in every field of neurosurgery, from when computer scientist Ivan Sutherland created “The Sword vascular pathology to craniosynostosis, to degenerative spinal of Damocles”—the first VR display system that provides an diseases and neuro-oncology.68,69 De Notaris et al. in 2011, immersive 3D experience.80 In modern-day surgical settings,

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FIGURE 6. Depiction of different modalities for interacting with volumetric anatomical models. A, Original specimen of a human skull. B, Side-by-side view of the volumetric model using virtual reality software. C, View of the same model on . D, 3D printed representation of the skull.

VR software and simulators have been adapted to provide the CONCLUSION user with interactive anatomical visualization that can include haptic feedback systems. However, simulators that adequately The challenge of learning the complexity and beauty of replicate patient-specific characteristics are currently in early neuroanatomy demands interacting with 3D information in a development.81 Additionally, VM can be explored via other way that helps one retain a dynamic comprehension of anatomical forms of extended reality, such as mixed reality or augmented correlations. Given the logistical difficulties and shortcomings reality—or even physically examined after 3D printing involved in relying solely on 2D representations of anatomy—SS (Figure 6). Recent technologies such as lightfield displays and VM models derived from dissections and surgeries could serve will allow us in the near future to expand the use of VM through as a valuable substitute. In the present paper, we have surveyed holographic representations of still or animated images operating the history of stereoscopy from antiquity to the modern era—and under the same principle of SS (Figure 7; Video).82 documented its ever-growing role in medical pedagogy. It is now The development of neuroanatomical VM repositories will incumbent on the medical community to not only continue inves- represent an invaluable source of education for medical students tigating new and improved methods of simulating anatomical and neurosurgical residents, and also an excellent opportunity features but to strive to find the best ways to deploy these for experienced neurosurgeons to interact with relevant anatomy resources in the academic setting and for the betterment of clinical using new, immersive technologies. practice.

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FIGURE 7. Holographic projection of a 3D scanned right hemisphere of a using a display.

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