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LITERATURE REVIEW J Neurosurg 127:192–198, 2017 T HE cranial nerves (CNs) have been studied since antiquity and assigned various nomenclature and numbering systems by anatomists such as Mari- nus, 11 Galen, 12 Vesalius, 34 Colombo, 4 Eustachius, 8 Fallo- pius, 9 Willis, 36 Vieussens, 35 and Soemmerring. 32 Since the 1778 work of 23-year-old medical student Samuel Thomas von Soemmerring (1755–1830), of Goettingen, Germany, CNs have been numbered from I to XII. 9,32 Soemmerring, who rose to become one of the most eminent anatomists by the turn of the 19th century, ranked the CNs accord- ing to their rostrocaudal exit points from the brainstem 19,32 (Fig. 1). His dissertation, De basi encephali et originibus nervorum cranio egredientium libri quinque (On the base of the brain and the origin of exits of cranial nerves in five books), became the basis for the universally accepted schema for numbering the CNs for more than 2 centuries. In it, Soemmerring notably proposed to separate the cra- nial nerves into 12 pairs, and to differentiate the facial and auditory nerves in giving them 2 different numbers, VII for the facial and VIII for the auditory nerve. 32 During the latter half of the 20th century, surgeons be- gan to microscopically visualize the brainstem exit zones of the CNs and their fine structure became a subject of interest. Details of the microanatomy, formerly of little practical consequence, were elucidated in great detail. The use of high-power microscopes in microsurgery provided a direct view of the fine neuronal structures in live patients with minimal anatomical distortion. Surprisingly, anatom- ABBREVIATIONS CN = cranial nerve; FIESTA = fast imaging employing steady-state acquisition. ACCOMPANYING EDITORIAL See pp 189–191. DOI: 10.3171/2016.3.JNS153041. SUBMITTED May 27, 2015. ACCEPTED December 29, 2015. INCLUDE WHEN CITING Published online October 28, 2016; DOI: 10.3171/2015.12.JNS151203. Perpetuation of errors in illustrations of cranial nerve anatomy C. Eduardo Corrales, MD, 1 Albert Mudry, MD, PhD, 2 and Robert K. Jackler, MD 2 1 Division of Otolaryngology–Head and Neck Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts; and 2 Department of Otolaryngology–Head and Neck Surgery, Stanford University School of Medicine, Stanford, California For more than 230 years, anatomical illustrations have faithfully reproduced the German medical student Thomas Soem- merring’s cranial nerve (CN) arrangement. Virtually all contemporary atlases show the abducens, facial, and vestibulo- cochlear nerves (CNs VI–VIII) all emerging from the pontomedullary groove, as originally depicted by Soemmerring in 1778. Direct observation at microsurgery of the cerebellopontine angle reveals that CN VII emerges caudal to the CN VIII root from the lower lateral pons rather than the pontomedullary groove. Additionally, the CN VI root lies in the ponto- medullary groove caudal to both CN VII and VIII in the vast majority of cases. In this high-resolution 3D MRI study, the exit location of CN VI was caudal to the CN VII/VIII complex in 93% of the cases. Clearly, Soemmerring’s rostrocaudal numbering system of CN VI-VII-VIII (abducens-facial-vestibulocochlear CNs) should instead be VIII-VII-VI (vestibuloco- chlear-facial-abducens CNs). While the inaccuracy of the CN numbering system is of note, what is remarkable is that generations of authors have almost universally chosen to perpetuate this ancient error. No doubt some did this through faithful copying of their predecessors. Others, it could be speculated, chose to depict the CN relationships incorrectly rather than run contrary to long-established dogma. This study is not advocating that a universally recognized number- ing scheme be revised, as this would certainly create confusion. The authors do advocate that future depictions of the anatomical arrangements of the brainstem roots of CNs VI, VII, and VIII ought to reflect actual anatomy, rather than be contorted to conform with the classical CN numbering system. https://thejns.org/doi/abs/10.3171/2015.12.JNS151203 KEY WORDS cranial nerve; anatomy; facial nerve; cochlear nerve; vestibulocochlear nerve; abducens nerve; perpetuation ©AANS, 2017 J Neurosurg Volume 127 • July 2017 192 Unauthenticated | Downloaded 08/01/20 11:35 PM UTC

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Page 1: Perpetuation of errors in illustrations of cranial nerve anatomy · LITERATURE REVIEW J Neurosurg 127:192–198, 2017 T he cranial nerves (CNs) have been studied since antiquity and

LITERATURE REVIEWJ Neurosurg 127:192–198, 2017

The cranial nerves (CNs) have been studied since antiquity and assigned various nomenclature and numbering systems by anatomists such as Mari-

nus,11 Galen,12 Vesalius,34 Colombo,4 Eustachius,8 Fallo-pius,9 Willis,36 Vieussens,35 and Soemmerring.32 Since the 1778 work of 23-year-old medical student Samuel Thomas von Soemmerring (1755–1830), of Goettingen, Germany, CNs have been numbered from I to XII.9,32 Soemmerring, who rose to become one of the most eminent anatomists by the turn of the 19th century, ranked the CNs accord-ing to their rostrocaudal exit points from the brainstem19,32 (Fig. 1). His dissertation, De basi encephali et originibus nervorum cranio egredientium libri quinque (On the base of the brain and the origin of exits of cranial nerves in

five books), became the basis for the universally accepted schema for numbering the CNs for more than 2 centuries. In it, Soemmerring notably proposed to separate the cra-nial nerves into 12 pairs, and to differentiate the facial and auditory nerves in giving them 2 different numbers, VII for the facial and VIII for the auditory nerve.32

During the latter half of the 20th century, surgeons be-gan to microscopically visualize the brainstem exit zones of the CNs and their fine structure became a subject of interest. Details of the microanatomy, formerly of little practical consequence, were elucidated in great detail. The use of high-power microscopes in microsurgery provided a direct view of the fine neuronal structures in live patients with minimal anatomical distortion. Surprisingly, anatom-

ABBREVIATIONS CN = cranial nerve; FIESTA = fast imaging employing steady-state acquisition.ACCOMPANYING EDITORIAL See pp 189–191. DOI: 10.3171/2016.3.JNS153041.SUBMITTED May 27, 2015. ACCEPTED December 29, 2015.INCLUDE WHEN CITING Published online October 28, 2016; DOI: 10.3171/2015.12.JNS151203.

Perpetuation of errors in illustrations of cranial nerve anatomyC. Eduardo Corrales, MD,1 Albert Mudry, MD, PhD,2 and Robert K. Jackler, MD2

1Division of Otolaryngology–Head and Neck Surgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts; and 2Department of Otolaryngology–Head and Neck Surgery, Stanford University School of Medicine, Stanford, California

For more than 230 years, anatomical illustrations have faithfully reproduced the German medical student Thomas Soem-merring’s cranial nerve (CN) arrangement. Virtually all contemporary atlases show the abducens, facial, and vestibulo-cochlear nerves (CNs VI–VIII) all emerging from the pontomedullary groove, as originally depicted by Soemmerring in 1778. Direct observation at microsurgery of the cerebellopontine angle reveals that CN VII emerges caudal to the CN VIII root from the lower lateral pons rather than the pontomedullary groove. Additionally, the CN VI root lies in the ponto-medullary groove caudal to both CN VII and VIII in the vast majority of cases. In this high-resolution 3D MRI study, the exit location of CN VI was caudal to the CN VII/VIII complex in 93% of the cases. Clearly, Soemmerring’s rostrocaudal numbering system of CN VI-VII-VIII (abducens-facial-vestibulocochlear CNs) should instead be VIII-VII-VI (vestibuloco-chlear-facial-abducens CNs). While the inaccuracy of the CN numbering system is of note, what is remarkable is that generations of authors have almost universally chosen to perpetuate this ancient error. No doubt some did this through faithful copying of their predecessors. Others, it could be speculated, chose to depict the CN relationships incorrectly rather than run contrary to long-established dogma. This study is not advocating that a universally recognized number-ing scheme be revised, as this would certainly create confusion. The authors do advocate that future depictions of the anatomical arrangements of the brainstem roots of CNs VI, VII, and VIII ought to reflect actual anatomy, rather than be contorted to conform with the classical CN numbering system.https://thejns.org/doi/abs/10.3171/2015.12.JNS151203KEY WORDS cranial nerve; anatomy; facial nerve; cochlear nerve; vestibulocochlear nerve; abducens nerve; perpetuation

©AANS, 2017J Neurosurg Volume 127 • July 2017192

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ical variations of the exit of certain CNs were recognized to not conform to the usual depiction in contemporary anatomical atlases.2 These observations, which included differences in the position of the nerve exit points from the pons and medulla, as well as their rostrocaudal position-ing, were particularly evident for the abducens, facial, and vestibulocochlear nerves (CNs VI–VIII, Fig. 1).

The purpose of this study is 3-fold. First, to investi-gate the current CN numbering system and its diffusion throughout the last 2 centuries, specifically analyzing CNs VI–VIII. Second, to perform a quantitative radiological study using MRI to determine the position and exit points of CNs VI–VIII in live patients. And third, analyze the findings of the radiological study and compare them to the description of CNs depicted in contemporary anatomical atlases.

MethodsHistorical Research

A collection of historical and contemporary refer-ences of CNs VI–VIII was compiled, spanning from the 2nd century ad through the beginning of the 21st century (Table 1). Special attention was paid to those references, which followed Soemmerring’s 1778 treatise. Historical anatomical books and journals, relevant to CN numbering and their relative positions, supplemented our reference database.

MRI StudyOne hundred MR images were studied to quantify the

rostrocaudal positioning of the exits of CNs VI–VIII. Ad-ditionally, the exit position between CN VII and CN VIII was assessed. Fifty prospective and 50 retrospective MR images that included imaging of the basal cisterns and CNs were identified in a consecutive manner from our

FIG. 1. Soemmerring’s brainstem illustration of 1778. Soemmerring’s brainstem view (left) with inset showing the anatomical depiction of the abducens (VI), facial (VII) and vestibulocochlear (VIII) nerves (right).

TABLE 1. Anatomical atlases examined in this study

References

Galen, 2008 (quoting Marinus, circa 100 ad)Galen, 1956 (circa 130–201 ad)Vesalius, 1543Colombo, 1559Fallopio, 1562Eustachio, 1564Willis, 1664Vieussens, 1684Soemmerring, 1778Lizars, 1860Cunningham, 1903Pernkopf et al., 1980Grant et al., 1989Moore & Dalley, 1999Sobotta & McMurrich, 1927; Pabst et al., 2001Gilman et al., 2003Logan et al., 2004Ellis et al., 2005Schünke et al., 2007Rhoton, 2007Snell, 2008Woosley et al., 2008Kiernan, 2009Agur & Dalley, 2009Tank & Gest, 2009Jackler, 2009Netter & Hansen, 2011Rohen et al., 2011

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radiology database in November 2012. Approval was ob-tained from the Stanford University School of Medicine institutional review board.

Image ComparisonFast imaging employing steady-state acquisition

(FIESTA) sequences were obtained from both 1.5- and 3-T scanners (GE Healthcare) at a slice thickness of 0.5 mm and a scan field of view of 160 mm. FIESTA imaging was used because it provides very high signals from tis-sues with T2/T1 ratios, providing more detailed informa-tion of CNs. The image matrix in pixels was 512 × 512, and voxel size (resolution) was 0.05 mm. Software used for analysis, reformatting, and quantification was Aquarius Intuition (TeraRecon Inc.). Three-dimensional modeling and volume rendering was performed using Vitrea Core Enterprise Solution (Toshiba, Inc.) and Aquarius Intuition. First, alignment for axial symmetry in relation to the inter-nal auditory canals was performed using angled lines on the coronal projection. The sagittal projection was used to complete the coronal alignment to be parallel to the pos-terior margin of the pons/brainstem. Using cross-section indicators, exit points of CN VI and CN complex VII/VIII were identified. The distance tool was used to measure be-tween these two locations. If the rostrocaudal distance was less than 0.25 mm, CN VI was classified as equal (i.e., be-ing at the same level) to CN complex VII/VIII.

ResultsSoemmerring’s 1778 CN Classification

The great majority of contemporary anatomical texts use illustrations rather than photographs to depict the brainstem entry and exit points of the CNs. A review of

contemporary atlases showed that nearly all works emu-late the 1778 anatomical arrangement of Soemmerring in which the rostrocaudal sequence is abducens (VI)-facial (VII)-vestibulocochlear (VIII) nerves (Fig. 2). In a few at-lases, the relation between CN VI and the CN VII/VIII complex is anatomically correct, although the nomencla-ture still follows Soemmerring’s classification (Cunning-ham5 and Lizars17). Of all anatomical illustrated referenc-es analyzed, only Cunningham’s depicted CN VII caudal to CN VIII.5

Quantitative MRI Study of CNs VI, VII, and VIIIAmong the 100 MR images studied, the exit location of

CN VI was caudal to the CN VII/VIII complex in 93%, equal to this complex in 3%, and rostral to this complex in 4% (Fig. 3). Furthermore, the exit position of CN VII was caudal to CN VIII on multiple MR images, although the resolution was not sufficient for analysis.

Comparison Between the MRI Study and the CNs Depicted in Contemporary Anatomical Atlases

A close inspection of Soemmerring’s 1778 depiction shows that CN VI is positioned approximately 2 mm ros-tral to the CN VII–VIII exit. When compared with high-resolution MR images showing the CN VI exit to be an average of 2 mm caudal to the CN VII/VIII complex, So-emmerring’s depiction spans the considerable distance of approximately 4 mm. In rare examples, such as Lizars’ atlas of 1860 and Cunningham’s atlas of 1903, they come much closer to actual anatomy than Soemmerring’s cus-tomary depiction.5,17 In only a few specialized atlases that are based upon direct microsurgical observation do the illustrations show the anatomically accurate vestibu-locochlear (VIII)-facial (VII)-abducens (VI) rostrocau-

FIG. 2. Comparison between Soemmerring’s and Netter’s brainstem view. Netter’s brainstem illustration (right) demonstrates the typical contemporary depiction of exit zones of CNs VI, VII, and VIII, analogous to Soemmerring’s brainstem view (left). Numbers represent the CN depicted. Copyright 2016 Elsevier Inc. All rights reserved. www.netterimages.com. Figure is available in color online only.

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dal sequence.15,25 In addition, Soemmerring’s illustration shows CN VII to be rostral to CN VIII. Actually, CN VII brainstem entry is caudal to CN VIII. Multiple MR im-ages analyzed coupled with microsurgical experience in this anatomical region indicates that CN VII enters the pons caudal to CN VIII (Figs. 4 and 5).

DiscussionVirtually all illustrations in the contemporary atlases

analyzed characteristically show CNs VI, VII, and VIII all emerging from the pontomedullary groove, which is the prominent sulcus on the ventral aspect at the junction between the pons and the medulla. This groove is drawn as a sulcus that protrudes most at the midline near the CN VI origin and slopes downward laterally. Placing the ori-gins of all 3 nerves in the sulcus may have been a conve-nient artistic device that could be used to align the artist’s illustration with the classic numbering system. Contrary to these illustrations, at microsurgery, CNs VII and VIII do not exit from a sulcus, but rather from the smooth sur-face of the lower lateral pons (Fig. 5). This anatomical de-tail is also readily apparent on MRI.10 CN VI, which exits from the anterior pontine surface, does arise from the pon-tomedullary sulcus. Published photographs of the ventral aspect of the brainstem agree with the surgical observa-tion that CNs VII and VIII emerge from the lower pons rather than the pontomedullary groove.26,37 One possible source of misclassification is the perspective from which the brainstem is viewed. Some illustrations depict the brainstem from an inferior perspective rather than from an anterior one. Gazing ventrally along the axis of the spi-

nal cord toward the undersurface of the brain can give the illusion that the CN VI exit is rostral to CN VII and VIII.18

Given the crude tools Soemmerring was working with, it should not be surprising that his sketches contained some errors. He worked with desiccated postmortem specimens that may well have been damaged through traumatic har-vesting. He had, at best, crude optical magnification sys-tems. While Soemmerring’s dissertation did not specify the number of specimens he studied, it does make clear that it involved dissections of a number of cadavers.32 It is conceivable that the specimen he chose for illustration was one of the rare examples in which the CN VI exit is actual-ly slightly rostral to that of the CN VII/VIII complex (4% in the present study). The MRI measurement technique used in the present study also has its limitations.3,6,28,29 Re-liable measurement of the distance between the exit of CN VI and the CN VII/VIII complex was possible, but not dis-cernment of the rostrocaudal arrangement between CNs VII and VIII. Only a few of the MR images analyzed pro-vided adequate T2/T1 ratios allowing for discernment of this arrangement (Fig. 3). Analysis of this relationship was possible through direct microsurgical observation, which, although qualitative in nature, reliably placed the CN VII exit caudal to CN VIII (Fig. 5).

To accept something as true, regardless of evidence, is not a characteristic of the scientific method. It is interest-ing to speculate what led these authors to override their instincts and training. Human intellectual thought is often influenced by beliefs instilled by our teachers and accepted as truth. The tendency to respect what is widely known can make us doubt the validity of personal observations when they are at variance with what we have learned. Perhaps in

FIG. 3. Brainstem 3D reconstruction of MR images from our database. CN VI is depicted in blue, CN VII in green, and CN VIII in red. The arrowhead and arrow represent the levels of CN VI (arrowhead) and VII (arrow) entry in all 4 images. A–C: Reconstruc-tions of a single MR image from our database represented in different angles. The coronal plane is reconstructed in panel A. The sagittal view is reconstructed in panel B. An inferior-oblique view of a 3D reconstruction is shown in panel C. The view is at the level of the pontomedullary junction showing CN VI arising from the junction. CNs VII and VIII are shown arising from the lower pons. Note that CN VII is caudal to CN VIII. D: This represents a separate MR image in a lateral oblique angle showing CNs VI, VII, and VIII in the lower pons and pontomedullary junction. Note that CN VII is caudal to CN VIII, and CN VI is caudal to the CN VII/VIII complex. Figure is available in color online only.

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the case of CNs it stems from a cultural acceptance of the dictum that “there is nothing left to be discovered in gross anatomy.”

The uncritical acceptance of anatomical renderings may originate from how anatomy is taught. From the earli-est stages of education, the numbering system of the CNs is deeply ingrained in the intellectual DNA of physicians and anatomists. Memorized through the use of colorful mnemonics, the rank order is recited repetitively until it becomes firmly set into memory.

Some educators, such as G.A. Petsko of Brandeis Uni-versity in his critique of dogma, perceived a value for it in the training of scientists: “Still, dogmas have their uses. Students find them very helpful. They provide a convenient encapsulation of the perceived wisdom of the moment.”24 This style of rote learning may have fixed the sequence of the CNs as an absolute and immutable truth and thus exempted it from critical analysis.

An inference from this study is that some scholars may well have preferred altering their anatomical depictions so that they align with the classical CN numbering system, even when they knew that it would mean that their illustra-tions would be at variance with their own direct anatomical observations. If true, the distortions were not mere tweaks, but rather necessitated major reconfiguration of the loca-tion of the roots of 3 CNs as they exit from the brainstem. It could be speculated that, loath to challenge the orthodox teaching, they preferred to distort their anatomical draw-ings rather than risk criticism that their drawings were at variance with the universal numbering system.

The question arises as to whether it would be wise or

prudent to revise Soemmerring’s CN classification scheme to more accurately reflect anatomy. Revising a universally recognized numbering scheme would certainly create con-fusion, especially in transition. What is clear, however, is that future depictions of the anatomical arrangements of the brainstem exits of CNs VI–VIII ought to reflect accu-rate anatomy, even though it will remain at variance with the classical numbering system (Fig. 4). This long-prop-agated error in the traditional numbering system of CNs teaches a lesson about fallibility in science. Inevitably, fu-ture observers will uncover misperceptions in 21st century descriptions due to limitations in our current technology and/or our present level of scientific understanding. One can only hope that future observers will be charitable when judging our errors and will consider them to be based upon incomplete knowledge rather than lack of rigor.

One might criticize our study on several grounds. One limitation is the lack of definite cadaveric analysis. This path was not pursued due to newer technology being avail-able, such as high-resolution MRI. Cadaveric dissection would still require multiple processing methods likely to distort our anatomical study. Indeed, it would require spe-cialized equipment to study this anatomical region without stretching the nerves from the brainstem. Likewise, the dis-sected, dehydrated, and fixed cadaveric specimens might also reveal nerve tract pathways not usually observed in a living human being. As noted above, high-resolution MRI had insufficient resolution to discern the arrangement be-tween CNs VII and VIII, but was clear to visualize the relationship between CN VI and the CN VII/VIII com-plex. But we felt confident that the radiological evidence

FIG. 4. Brainstem illustration depicting the proximal courses of CNs VI, VII, and VIII (left) compared with their actual anatomical arrangement (right). Copyright Robert K. Jackler. Published with permission. Illustration by Christine Gralapp. Figure is available in color online only.

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on some MR images coupled with the quantitative surgi-cal experience was sufficient to determine the anatomi-cal variance observed. Selection bias may also affect our results, as we chose multiple, well-known, contemporary references, but it was not all inclusive. And finally, our data support new information regarding the CN anatomy due to newer technology at our disposition. It does not, howev-er, reproach past anatomists and illustrators for distorting anatomy. They did their best with the tools and techniques available to them.

Most scientists would agree with the statement “dogma has no place in science” as it requires acceptance of beliefs that are not firmly rooted in evidence. When faced with an incongruity between actual human structure and an arbitrary numbering system, the logical scientific choice should be the option based in observable reality. The more than two-century tradition of inaccurate anatomical draw-ings illustrates that even scientists may be susceptible to the comforting allure of traditional thought, with its poten-tial to suppress critical thinking. Perhaps it could be said that the most dogmatic rule in science and medicine is that dogma is alive and well in both fields. An awareness of the ingrained tendency of human thought to give excessive reverence to the familiar should help maintain openness to alternative interpretations of widely held “truths.”

ConclusionsVirtually all illustrations of contemporary atlases ana-

lyzed characteristically show CNs VI, VII, and VIII all emerging from the pontomedullary groove as originally depicted by Soemmerring. As shown by our MRI find-ings, the exit location of CN VI was caudal to the CN VII/VIII complex in 93% of cases. Furthermore, multiple MR images analyzed coupled with microsurgical experience of this anatomical region indicate that CN VII enters the pons caudal to CN VIII. Revising a universally recognized numbering scheme would certainly create confusion, es-pecially in transition. What is clear, however, is that future depictions of the anatomical arrangements of the brain-stem exits of CNs VI–VIII ought to reflect accurate anato-my, even though it will remain at variance with the classic numbering system.

AcknowledgmentsWe thank Drs. Nancy Fischbein and Shannon Walters for tech-

nical guidance on the imaging aspect of this study, and Christine Gralapp for illustrations.

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FIG. 5. A–C: Surgical endoscopic view of the root exit zones of CNs VI, VII, and VIII in 3 separate MR images (courtesy of Jacques Magnan). In panel B, there is a prominent anterior inferior cerebellar artery (AICA). D: An interpretative illustration of panel C. Copyright Robert K. Jackler (panel D). Published with permission. Illustration by Christine Gralapp. Figure is available in color online only.

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DisclosuresThe authors report no conflict of interest concerning the materi-als or methods used in this study or the findings specified in this paper.

Author ContributionsConception: Jackler. Design: all authors. Acquisition of data: Corrales, Mudry. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Jackler. Statistical analysis: Corrales, Mudry. Administra-tive/technical/material support: Corrales, Mudry. Study supervi-sion: Jackler.

CorrespondenceRobert K. Jackler, Department of Otolaryngology-Head and Neck Surgery, Stanford University School of Medicine, 801 Welch Rd., Stanford, CA 94305. email: [email protected].

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