文献导读 |Rhoton显微神经外科解剖学遗产-跨越50年之演进与转化的分析
来源：楠阅读（微信号neurosurgeon-nan）
the microneurosurgical anatomy legacy of albert l. rhoton jr., md: an analysis of transition and evolution over 50 years
作为显微神经外科解剖学研究的先驱，albert l. rhoton jr.给这一不断拓展的领域带来的是激动与领悟。
他所做工作的影响已经被公认为神经外科历史上的基石之一，得以促使全球神经外科医生的手术都变得更加安全与微创。
rhoton医生先后率领他的119位研究员和4位医学插画师（bob beach、carla lenkey、david peace和margaret e. “robin” barry）共同发表了大量优秀著作，已经被汇编于教科书《cranial anatomy and surgical approaches》和网站“the rhoton collection”之中。然而，他的研究思想在数十年间的演变过程却并不为世人所熟知。我们作为他曾经的研究员的代表，在本文中基于历史的视角回顾了他的大量著作，并且探讨了显微神经外科解剖学研究的前景。
as a pioneer of the study of microneurosurgical anatomy, albert l. rhoton jr. brought excitement and understanding to this expanding field. the impact of his work has been heralded as one of the cornerstones in the history of neurosurgery that led to safer and gentler surgical treatment by neurosurgeons all over the world. a large number of excellent works published by dr. rhoton, his 119 fellows, and 4 medical illustrators (bob beach, carla lenkey, david peace, and margaret e. “robin” barry) were compiled into the textbook cranial anatomy and surgical approaches and “the rhoton collection” (fig. 1, tables 1 and 2). however, the process by which his research ideas evolved over the years is not well known. in this article, we review his numerous works from a historical perspective, on behalf of all his former research fellows, and discuss future prospects for microneurosurgical anatomical research.
我们复习了过去50年间编撰的大约500种出版物，其中包括了160余篇重要的原创性文章。然后，按照时间顺序将其划分为5个阶段，分别对每个阶段进行解读，并且对第一阶段的划时代研究作了较为详细的论述。此外，《journal of neurosurgery》的部分封面曾经刊发了rhoton医生及其研究员所撰手稿的插图，我们展示了其中一些具有重要历史意义的研究课题的插图以供读者参阅。
we reviewed approximately 500 publications written during the last 50 years, including over 160 major original articles, and then divided them chronologically into 5 stages. each stage is explained individually, and the epoch-making studies of the first stage are discussed in some detail. the front covers of the journal of neurosurgery issues with the figures from the manuscripts written by dr. rhoton and his fellows and some figures representing the features of the historically important projects are shown for visual reference (figs. 2 and 3).
显微神经外科解剖学的萌芽
dawn of microneurosurgical anatomy
和很多先驱一样，rhoton医生在开展研究之初，也是不得不工作在一个极不理想的环境之中。20世纪60年代后期，他在罗切斯特市梅奥医学中心任职的时候，即开始使用猴子进行颅神经的临床解剖学研究。随后，又借助尸检标本的脑和颞骨，重点报道了颅神经变异的详尽解剖。他作此选择的一个原因是颅神经走行于颅底和脑干表面。
as is the case with many pioneers, dr. rhoton had to work in an environment that was far from optimal when he performed his initial research. while a member of the staff at the mayo clinic in rochester in the latter half of the 1960s, he began his anatomical study of the cranial nerves (cns) for clinical purposes using monkeys. then, using autopsy brains and temporal bones, he focused his reporting on the detailed anatomy of the cranial nerves with variations (fig. 3a). one of the reasons for his choice was that the cranial nerves coursed on the surface of the brainstem and skull base.
1972年，rhoton医生移居佛罗里达州盖恩斯维尔市，被聘任为佛罗里达大学外科学系的神经外科主任。1975年，他仰仗数笔慈善捐款建立了theodore gildred显微神经外科实验室，用于开展研究和教学。通过研发与完善人体尸头标本动静脉彩色乳胶灌注系统，以及出自艺术家之手的绘图和经过修描的照片，他借助其出版物建立了一套可视化的和易于理解的显微外科解剖学新标准。
装备精良的实验室也使得他能够更加精细地聚焦于诸如如何更安全地治疗垂体肿瘤和听神经瘤患者等自己感兴趣的手术领域。rhoton医生还热衷于研究同时代世界各地其他神经外科医生的手术技巧，尤其对m. gazi yaargil医生的手术及其所发表的报告印象深刻，而且利用灌注尸头标本从解剖学视角详细审视了这些报告的内容。
in 1972, he moved to gainesville, florida, and was appointed chief of the division of neurosurgery in the department of surgery at the university of florida. in 1975, thanks to several philanthropic contributions, he was able to establish the theodore gildred microneurosurgical laboratory, a facility for both research and education. by developing and refining a system of colored-latex injection of arteries and veins in human cadaveric specimens coupled with artists’ renderings and retouched photos, he set a new standard for visualizing and understanding microsurgical anatomy with his publications. the well-equipped laboratory also allowed him to focus in greater detail on his surgical areas of interest, such as the safer treatment of patients with tumors of the pituitary gland and acoustic neuromas. he was a keen student of the operative techniques of other contemporary neurosurgeons from around the world. he was particularly impressed by the operative and published reports of dr. m. gazi yaargil. utilizing his injected cadaveric specimens, dr. rhoton examined the contents of those reports in great detail from the anatomical point of view.
rhoton医生早期的巨著之一是听神经瘤手术中面神经的研究。在那个时代，此类肿瘤大多数只有在非常巨大的时候才会被发现，手术中经常损伤面神经。他在手术中发现，在解剖学上面神经经常被推移至肿瘤包膜的前半部分；而且先前有病理学家曾经报道过面神经前移。他指出，面神经前移系其大多走行于内听道前上方之故，而肿瘤通常起源于走行在内听道后方的前庭神经。他还建议了手术中探查面神经的两个区域，即内耳道开口处和神经根出脑干区。在这两个区域内，面神经尚未被肿瘤显著推移，神经成分的原始解剖关系很可能保持不变。这项研究有助于听神经瘤手术中保存面神经，引起了其他神经外科医生的关注。
rhoton医生还开展了针对经皮立体定向射频毁损术的三叉神经研究，针对视神经减压术的视神经研究，以及针对舌咽神经痛和颈静脉孔区肿瘤治疗的颈静脉孔和后组颅神经研究。当时彩色幻灯片的制作成本很高，因此研究期间只拍摄了黑白照片。rhoton医生请他的医学插画师对黑白照片进行了润色，帮助读者标清关键结构。经过修描的照片清晰地显示了原始光面照片无法显示的所有重要细节。
one of his great works in the earliest stage was his study of cn vii for acoustic neuroma surgery. in those days, most of these tumors were not found until they were very large, and cn vii was often damaged during surgery. he found anatomically at surgery that cn vii was often stretched over the anterior half of the tumor capsule; its anterior shifting had previously been pointed out by pathologists. he stated that the anterior shift of cn vii was because it mostly coursed in the anterosuperior part of the internal auditory canal, while the tumor usually originated from the vestibular nerves coursing in the posterior part of the canal (fig. 3b). he also suggested 2 regions for finding cn vii intraoperatively, namely, in the lateral end of the internal auditory canal and the nerve’s brainstem exit zone. in these 2 regions, cn vii was not displaced markedly by the tumor, and the original anatomical interrelation of neural components was likely to be maintained. this study benefited the efforts to preserve cn vii during acoustic tumor surgery and attracted the attention of other neurosurgeons. dr. rhoton also studied the trigeminal nerve for the purpose of percutaneous stereotactic radiofrequency lesioning, the optic nerve for optic nerve decompression, and the jugular foramen and the lower cranial nerves for the treatment of glossopharyngeal neuralgia and jugular foramen tumors. at that time, because making color slides was costly, only black-and-white photographs were taken during the research. dr. rhoton asked his medical illustrators to retouch black-and-white photographs to clarify critical structures to help the reader. the retouched prints clearly showed all the important details that the original glossy prints would have failed to display.
自20世纪60年代末开始，垂体肿瘤经蝶手术进展迅速。rhoton医生研究了鞍区和海绵窦的解剖，阐明了蝶鞍前壁鼻中隔附着处和海绵窦间静脉连接等的变异。此外，他还研究了蝶窦外侧壁，确定了颈动脉隆突，并且报道了其厚度和缺如概率。在这些报告中，他汇集并重新整理了经蝶手术所需的解剖学知识，并提供了彩色图解和经过修描的黑白照片。近年来，随着从显微镜到内镜的技术改进，如此而得的解剖学知识对于各种经鼻入路的最新进展作出了巨大贡献。
transsphenoidal surgery for pituitary tumors progressed rapidly starting in the late 1960s. dr. rhoton studied the anatomy of the sellar region and cavernous sinus. he clarified variations of the septal insertion on the anterior floor of the sella turcica and those of the intercavernous venous connections. he furthermore studied the lateral surface of the sphenoid sinus and pointed to the carotid prominence (bulging of the internal carotid artery [ica]), and reported on its thickness and the frequency of its defects. in these reports he accumulated and reorganized the anatomical knowledge necessary for transsphenoidal surgery, providing color illustrations and retouched black-and-white photographs (fig. 3c). the anatomical knowledge thus obtained has contributed greatly to recent advances in various transnasal approaches, as techniques evolved in recent years from microscopic to endoscopic.
与颅内动脉瘤直接夹闭手术的发展同步，rhoton医生于20世纪70年代末还开始了一系列关于动脉及其穿支的研究课题。他首先研究了大脑前-前交通-回返动脉复合体，而且经常会在讲座中提问heubner回返动脉起自哪一部分。其中有关基底动脉上段及其穿支的课题，为难度较大的基底动脉瘤夹闭手术提供了巨大的帮助。另外，该系列研究还拓展至脉络膜前动脉、m1段血管穿支和颈内动脉颅内段及其穿支。关于颈内动脉床突以上的部分，他提出了一种新的分段方法：分别基于眼动脉、后交通动脉和脉络膜前动脉的起始位置，划分为眼动脉段、交通动脉段和脉络膜动脉段。
如果认为有必要使读者更加明了，他会毫不犹豫地重新分类或创建新的命名。他还在该系列研究中最终从3个方面演示了囊性动脉瘤的解剖。这些外科解剖学研究成果给神经外科医生们提供了极大的帮助，先前他们只能通过神经放射科医生撰写的论文和教科书，或者基于血管造影的发现研究动脉及其分支的解剖。在这一系列的研究中，rhoton医生及其研究团队开始使用动脉内注射红色丙烯酸或乳胶的方法，以便于血管分支的解剖。
in accordance with the development of direct clipping for intracranial aneurysms, dr. rhoton also started a series of projects on arteries and their perforators in the late 1970s. he first studied the anterior cerebral–anterior communicating–recurrent artery complex, and in his lectures he often asked which portion the recurrent artery of heubner originated from (fig. 3d). the project on the upper basilar artery and its perforators was of great help for clipping difficult basilar aneurysms. rhoton extended this series to the anterior choroidal artery, perforators from the m1 segment, and the intracranial ica and its perforators. regarding the supraclinoid portion of the ica, he suggested a new segmentation: ophthalmic, communicating, and choroidal segments based on the site of origin of the ophthalmic, posterior communicating, and anterior choroidal arteries, respectively. he did not hesitate to reclassify or coin new names if he thought it necessary for readers to have more clarity. in this series, he finally presented 3 facets of the anatomy of saccular aneurysms. the results of these studies on surgical anatomy enormously benefited neurosurgeons who had previously been able to study the anatomy of the arteries and their branches only through papers and textbooks written by neuroradiologists and based on angiographic findings. for this series, rhoton and his group began using the injection of red-colored acrylic or latex into arteries to facilitate dissection of branches.
20世纪70年代，手术显微镜开始被用于微血管减压术治疗三叉神经痛。当rhoton医生开始关注这一手术的时候，他在显微外科实验室中针对后颅窝，特别是小脑桥脑角内颅神经与动脉血管的解剖关系进行了一系列深入研究。这些研究对于全球神经外科医生更加安全地实施后颅窝手术多有裨益。最初的研究聚焦于小脑上动脉和三叉神经的关系，以及其与三叉神经痛的潜在因果联系。由于当时尚不清楚面神经根出脑干区动脉减压的重要性，因此接下来的研究课题较多地关注于小脑前下动脉-面神经-位听神经复合体的研究。为阐明面肌痉挛的解剖基础，随后又开展了面神经根出脑干区与相关动脉之间关系的研究。
in the 1970s the operative microscope began to be used for the treatment of trigeminal neuralgia via microvascular decompression (mvd). as dr. rhoton began to focus on the operative procedure, he instituted an in-depth series of studies in the microsurgical laboratory of the anatomical relationships between cranial nerves and arteries in the posterior fossa, especially in the cerebellopontine angle. these studies have aided neurosurgeons throughout the world to more safely perform surgery in the posterior fossa. the first study focused on the relationships of the superior cerebellar artery to cn v and its potential causal relationship with trigeminal neuralgia. much attention was paid to the study of the anterior inferior cerebellar artery–cn vii-viii complex in the next project, since the importance of arterial decompression at the exit zone of cn vii was not well known at that time. to clarify the anatomy of hemifacial spasm, the relationships between the exit zone of cn vii and the related arteries were later examined.
为了便于学习和记忆解剖学关系，rhoton医生以制定解剖学“原则”而闻名。通过这些研究，他开始倡导“3原则”，以有助于对后颅窝基本解剖结构，如小脑外表面、脑干、小脑脚、小脑-脑干裂、小脑动脉和静脉的理解。这一原则包括小脑桥脑角内的3组神经血管复合体：其上部的滑车神经、三叉神经及小脑上动脉，中部的面神经、位听神经及小脑前下动脉，下部的后组颅神经和小脑后下动脉。以上3组结构涉及三叉神经痛、面肌痉挛和舌咽神经痛等血管压迫综合征。其中一位作者（t.m.）在微血管减压术中应用“小脑桥脑角3原则”，将枕下外侧入路分为3种：显露三叉神经的外侧幕下小脑上入路、显露面神经根出脑干区的小脑绒球下入路和显露舌咽神经的髁窝入路。
to facilitate learning and retention of anatomical relationships, dr. rhoton was well known for making “rules” of anatomy. through these studies, he started to advocate the “rule of 3” as an aid to understanding the basic anatomy of the posterior fossa, including the cerebellar surfaces, brainstem, cerebellar peduncles, cerebellar-brainstem fissures, cerebellar arteries, and veins. this rule includes 3 neurovascular complex groups in the cerebellopontine angle: cns iv and v and the superior cerebellar artery in the upper portion, cns vii and viii and the anterior inferior cerebellar artery in the middle portion, and the lower cranial nerves and the posterior inferior cerebellar artery in the lower portion. these 3 groups are involved in the vascular compression syndromes trigeminal neuralgia, hemifacial spasm, and glossopharyngeal neuralgia. one of the authors (t.m.) applied the “rule of 3 in the cerebellopontine angle” in his mvd surgeries and divided the lateral suboccipital approach into 3 approaches: the infratentorial lateral supracerebellar approach to the trigeminal nerve, the infrafloccular approach to the exit zone of the facial nerve, and the transcondylar fossa approach to the glossopharyngeal nerve.
rhoton医生引用率最高的5篇论文中的4篇撰写于第一阶段。这些论文的内容在当时是非常新颖的，许多神经外科医生都认为十分重要。
four of dr. rhoton’s 5 most-cited papers were written during the first stage (table 3). the contents of those papers were very new then and considered very important by many neurosurgeons.
服务于普通神经外科学的显微解剖
study of basic microneurosurgical anatomy for general neurosurgery
20世纪80年代，rhoton医生将其研究拓展至其他解剖部位及结构，包括脑室、静脉、枕骨大孔、小脑幕切迹和脑池。
正如他最初设想的那样，这是一个“制图”的过程。在rhoton医生开展研究之前，解剖学家编撰的教科书中主要描述重要神经结构与脑室的关系，几乎没有脑室相关血管的任何表述。
rhoton医生收集了解剖学家所描述的脑室与神经结构和放射科医生所描述的血管结构的信息，并且更多地以其在神经外科手术中的重要性为主线，站在神经外科视角上对其进行了重新整理。
rhoton医生在这些关于脑室的课题中，不仅聚焦于显微外科解剖学，还关注到手术入路。他首先针对第三脑室进行研究，并且在两篇论文中报道了他的研究结果：第一部分涉及显微外科解剖学，第二部分则涉及手术入路。在后续关于第四脑室的研究课题中，最初的显微外科解剖学论文发表之后，他和其中一位作者（t.m.）还曾试图再发表一篇有关手术入路的论文，但是当时除中线经小脑蚓部入路之外并未述及其他入路。
rhoton医生通过标本的分步解剖对第四脑室的背侧显露进行了验证，并且阐明了小脑延髓裂的解剖结构，进而提出了一种全新的革命性手术入路。
目前，这一众所周知的所谓经小脑延髓裂入路或膜髓帆入路的新入路正在被广泛使用。上述两种命名均出自该解剖学研究课题，都是我们在实验室内外经过讨论后确定的。rhoton医生在有关侧脑室的课题中，最为关注脉络膜裂，提出了经由该裂隙的安全入路；随后更为深入地研究了经由脉络膜裂的手术入路，并且进行了单独报道。
in the 1980s, dr. rhoton extended his studies to other anatomical regions and structures, including the ventricles, the veins, the foramen magnum, the tentorial incisura, and the cisterns. this was a “mapmaking” process as he initially envisioned it. prior to dr. rhoton’s studies, the relationships of important neural structures to the ventricles had been primarily described in textbooks written by anatomists. there had been hardly any descriptions of blood vessels related to the ventricles. he collected information on the ventricles and the neural structures described by anatomists and the vascular structures described by radiologists and reorganized them more along the lines of neurosurgical importance and perspective. in these ventricular projects, he focused not only on the microsurgical anatomy but also on surgical approaches. he first studied the third ventricle, reporting his results in 2 papers: part 1 focusing on microsurgical anatomy and part 2 on operative approaches. in the next project, which focused on the fourth ventricle, he and one of the authors (t.m.) also attempted to publish a paper on the operative approaches following an initial paper on microsurgical anatomy, but no approaches other than the midline transvermian approach were described at that time. the step-by-step dissection of the specimen to demonstrate the fourth ventricle from the posterior side, which also revealed the anatomy of the cerebellomedullary fissure, later brought the proposal of a new innovative approach. this new approach is now widely used and well known as the trans–cerebellomedullary fissure approach or the telovelar approach. both names were derived from this anatomical project and through our discussions in and outside the lab. in the lateral ventricle project, much attention was paid to the choroidal fissure, and a safe approach through that fissure was described; a further study on the surgical approach through the choroidal fissure was reported independently.
rhoton医生在研究静脉的早期阶段遭遇了因静脉壁薄易碎而致的技术性难题，但是在完成脑室相关课题的同时，静脉注射适宜技术的创建终获成功。rhoton医生最先选择研究的是后颅窝静脉。当时huang和他的同事们已经通过血管造影检查实现了静脉的完美可视化，并且对各支静脉进行了命名。
在此卓越的放射学研究基础上，rhoton医生调整了后颅窝静脉的命名，以便使其更加符合神经外科专业的理解。新的命名与rhoton医生的“3原则”一致。譬如，huang及其同事所命名的“小脑前中央静脉”被调整为“小脑中脑裂静脉”，“岩上静脉”被调整为“小脑桥脑裂静脉”，huang和wolf所命名的“侧隐窝静脉”被调整为“小脑延髓裂静脉”。紧随后颅窝静脉研究其后，rhoton医生还开展了关于岩上静脉复合体的研究课题。对于幕上静脉，他则将其划分为深部静脉系统和浅部静脉系统。
technical difficulties due to fragility of the thin venous wall were encountered in the early stages of the venous studies. eventually succeeding in establishing proper venous injection techniques while completing projects on the ventricles, dr. rhoton chose the veins of the posterior fossa to be studied first. huang and colleagues had reported excellent visualization of the veins during angiography studies and they had already named each vein. based on their remarkable radiological studies, the naming of the veins of the posterior fossa was reorganized in a way to be more suitable for neurosurgical understanding. the new naming was related to dr. rhoton’s rule of 3. for example, the vein referred to as “the precentral cerebellar vein” by huang and colleagues was changed to “the vein of the cerebellomesencephalic fissure,” the vein named “the superior petrosal vein” by huang et al. to “the vein of the cerebellopontine fissure,” and the vein called “the vein of the lateral recess” by huang and wolf to “the vein of the cerebellomedullary fissure.” the study on the veins of the posterior fossa was later followed by the projects on the superior petrosal venous complex. with regard to supratentorial veins, dr. rhoton grouped them into veins of the deep system and veins of the superficial system.
颅底外科学研究
study for skull base surgery
伴随自20世纪80年代中期至90年代初颅底外科学的发展，为了适应颅底入路的最新进展，rhoton医生再次开展了海绵窦、眶部、颞骨、颈静脉孔和枕骨大孔的研究。在此期间，他开始使用彩色照片和插图呈现各种术式的尸头分步解剖。
为回应20世纪80年代所倡议的处理颈动脉-眼动脉动脉瘤的硬膜内外联合直接入路（所谓的dolenc入路），rhoton医生研究了海绵窦及其邻近区域的各种手术入路。同样，为回应kobayashi等人所发表的关于颈动脉陷窝动脉瘤的报告，他又在研究中发现了“环绕颈内动脉床突段的硬膜环”。伴随经岩骨前/后入路的进展，颞骨也被重新研究，不仅验证手术入路，而且将岩上静脉复合体作为一个相关课题进行研究。
随着枕骨大孔侧方入路，如远外侧入路、极外侧入路、经髁入路和经髁窝入路等的进展，再次开展了枕骨大孔后外侧部分的研究，并且将当时提出的几种改良后外侧入路修订为经髁、髁上和髁旁入路。
颈静脉孔区是最困难的手术显露区域之一，耳鼻喉科医生和神经外科医生均曾针对此区域报道过许多入路，从而导致了一定程度的混乱和一些问题。在颈静脉孔区入路的发展进程中，rhoton实验室先后进行过3次解剖学研究，试图予以澄清。第一次是在1975年，主要局限于颅内一侧；第二次是在1997年，重点聚焦于颞骨内侧面的孔道部分；第三次是在2016年，回顾了已经提出的全部手术入路。
关于眶部则分别研究了经颅入路、侧方入路和眶上裂入路。此外，rhoton医生还针对颅面中部及正中颅底、单侧上颌骨次全切除手术入路和颅骨骨膜瓣的血管解剖结构进行了研究。
as skull base surgery evolved from the mid-1980s to the early 1990s, dr. rhoton again studied the cavernous sinus, orbit, temporal bone, jugular foramen, and foramen magnum for the newly developed skull base approaches. during this period he began to use color photographs and illustrations to present step-by-step cadaveric dissections of the various procedures. in response to the proposal in the 1980s of a combined epi- and subdural direct approach to carotid-ophthalmic aneurysms, the so-called dolenc approach, dr. rhoton studied the various surgical approaches to the cavernous sinus and adjacent regions (fig. 3e). also responding to the report of carotid cave aneurysms by kobayashi et al., he picked up “the dural collars and rings around the clinoidal segment of the ica” for the study. with the development of the anterior and posterior transpetrosal approaches, the temporal bone was again studied. not only were the surgical approaches demonstrated, but also the superior petrosal venous complex was studied as a related project. with the development of the lateral foramen magnum approaches, such as the far-lateral, extreme-lateral, transcondylar, and transcondylar fossa approaches, the posterolateral portion of the foramen magnum was again studied, and several modifications of the posterolateral approach thus far proposed were reorganized as the transcondylar, supracondylar, and paracondylar approaches. the jugular foramen is one of the most difficult regions for surgical access and many approaches to this region were reported by both otolaryngologists and neurosurgeons, which caused some confusion and problems. during the course of the development of the approaches to the jugular foramen, efforts were made to clarify them by anatomically studying them 3 times in the rhoton lab: first, in 1975, mainly on the intracranial side; second, in 1997, on the foraminal portion inside the temporal bone; and third, in 2016, reviewing all the proposed surgical approaches. regarding the orbit, the transcranial approach, the lateral approach, and the superior orbital fissure approach were studied separately. the midface and the midline skull base, the unilateral subtotal maxillectomy approach, and the vascular anatomy of the pericranial flap were also examined.
20世纪90年代末，rhoton医生对于三维成像产生了高度兴趣，认为其有助于更加准确地在颅底手术中判断深浅。在toshiro katsuta博士1993年-1995年做研究员期间，rhoton医生开始尝试在显微神经外科解剖进程中进行立体摄影。1998年，katsuta等在其关于颈静脉孔的文章中首次展示了三维投影图像。早期阶段，三维投影是通过使用经由两台幻灯机投影的两套幻灯片获得的。
进入21世纪后，经由国际研究员的帮助，三维投影在rhoton实验室迅猛发展，已经成为讲授颅底外科领域复杂手术解剖和理解脑内纤维形态的重要工具。2006年，shimizu等发布了详细的经典三维文献。他们使用两台水平式偏光滤镜幻灯机，在同一幅银幕上投射出立体像对，观众通过佩戴三维眼镜即可观看到立体影像。rhoton医生要求他的研究员重行颞骨解剖，以便进行三维展示，并且于2007年发表了全部均为三维图像的《anatomy and surgical approaches of the temporal bone and adjacent areas》，占据了整本《neurosurgery》增刊。2015年，martins等还综述了三维数字投影技术在神经外科教学领域的研究进展。
in the late 1990s, dr. rhoton became keenly interested in 3d imaging, which he believed would aid in more accurate understanding of depth during skull base procedures. during the fellowship of dr. toshiro katsuta from 1993 to 1995, dr. rhoton began to experiment with stereophotography of microneurosurgical dissection. katsuta et al. first presented the 3d projection figures in their article on the jugular foramen in 1998. in the early stage, 3d projection could be obtained by using a double set of slides, projected through 2 slide projectors. in the 2000s, 3d projection rapidly advanced at the rhoton lab with the assistance of international fellows. it became an important tool for teaching the complex anatomy of surgical fields in skull base surgery and for understanding intracerebral fiber topography. in 2006, shimizu et al. reported a detailed classic 3d documentation. two slide projectors with polarizing lens filters of horizontal type for each stereoscopic pair projection and a silver screen were used, and the audience members wore 3d glasses. dr. rhoton asked his fellows to dissect the temporal bone again for a 3d presentation, and it was published as “anatomy and surgical approaches of the temporal bone and adjacent areas” with all figures in 3d, occupying an entire supplemental issue of neurosurgery, in 2007. in 2015, martins et al. summarized the progress of 3d documentation describing 3d digital projection in neurosurgical education.
rhoton医生自1999年从佛罗里达大学神经外科主任的职位上退休以后，研究课题便不再仅局限于他自己的手术，而是涉及神经外科更为广泛的领域。最终，他又将研究选题留给了每一个研究员。
after his retirement from the chairmanship of the department of neurosurgery at the university of florida in 1999, the topics of his research projects became less focused on his own surgeries and were taken from broader fields of neurosurgery. eventually he left the selection of research topics to each fellow.
借助神经纤维解剖的脑内结构研究
study of the internal structure of the brain by fiber dissection technique
rhoton医生已经开始使用纤维解剖技术研究脑的内部结构，以便回应ture及其同事对klingler旧有的纤维解剖方法的改进。从借助纤维解剖技术开展视辐射的三维研究开始，rhoton医生进行了一些包括或不包括弥散张量成像的研究。伴随脑干手术的进展，他的研究又拓展至脑干纤维解剖，特别是安全手术入路区域。随着神经外科的多样化，纤维解剖技术已经用于包括听觉脑干植入和脑深部刺激等在内的众多领域的研究。
dr. rhoton began to study the internal structures of the brain using a fiber dissection technique in response to ture and colleagues’ revitalization of klingler’s old method of fiber dissection. starting with a 3d study of the optic radiation by fiber dissection, several studies were undertaken with or without accompanying diffusion tensor imaging. with the development of brainstem surgery, his studies extended to the anatomy of the brainstem fibers, especially with respect to the safe entry zone. in accordance with the diversification of neurosurgery, the fiber dissection technique has been applied to the study of various fields, including auditory brainstem implantation and deep brain stimulation.
服务于新技术的手术解剖学
surgical anatomy combined with new advanced technologies
截至20世纪末，显微神经外科早已成熟。21世纪初，神经外科治疗进一步多样化。因此，rhoton实验室设计了一些课题以满足新的手术方式的需求。譬如，包括内镜手术在内的微创或无创手术，以及与神经导航系统、血管内介入手术、听觉脑干植入和脑深部刺激等各种技术的协同。部分课题则旨在避免某些手术中发生的并发症。至于内镜手术，不只是经鼻内镜手术，而且针对动脉瘤和小脑桥脑角病变的内镜辅助手术也进行了详尽的解剖学研究。
by the end of the 20th century, microneurosurgery had matured, and in the early 21st century neurosurgical treatment became further diversified. accordingly, in the rhoton lab several projects were created to meet the demands of new surgical modalities, such as less or minimally invasive surgery including endoscopic surgery, collaboration with various technologies including the neuronavigation system, endovascular surgery, auditory brainstem implantation, and deep brain stimulation. some projects were designed to avoid surgical complications during certain surgical procedures. in the case of endoscopic surgery, anatomical studies were made in detail not only for endonasal endoscopic surgery but also for endoscopeassisted surgery for aneurysms and cerebellopontine angle lesions.
rhoton医生接收了来自很多不同国家和专业的研究员，其中包括整形外科医生和耳鼻喉科医生，他们也将各自领域的不同文化和新观念带进了rhoton实验室。rhoton医生为全球神经外科教育领域作出了巨大成绩，在很多国家进行过多次讲座，并且开设过大量实操课程。出于教学的目的，他还凭借rhoton实验室的解剖研究制作了颅底及颅神经的三维互动模型。目前，“the rhoton collection”正在美国神经外科医师协会（aans）的网站上持续更新。
dr. rhoton accepted research fellows from many different countries and disciplines, including a plastic surgeons and otolaryngologists, who brought different cultures and new ideas from their fields to the lab. he made tremendous efforts in the education of neurosurgeons all over the world, giving countless lectures and holding many handson courses in various countries. the 3d interactive model of the skull base and cranial nerves for educational purposes was also made from the anatomical studies in the lab. the rhoton collection is being continuously updated on the american association of neurological surgeons (aans) website.
前景展望
future prospects
很多人可能认为，rhoton医生编写的教科书《cranial anatomy and surgical approaches》出版之时，显微神经外科解剖学研究既已逼近终点。但是，本文作者坚信，未来仍有更多的课题需要研究。教科书中的内容是2002年之前大约36年的研究成果。在接下来的14年里，rhoton实验室又发表了80余篇新颖的解剖学论文，我们在第四和第五阶段所描述的主题中尚未将其全部囊括其中。
many people may have thought that microneurosurgical anatomical study was nearly complete when dr. rhoton’s textbook, cranial anatomy and surgical approaches, was published. the authors believe, however, that there are still many more projects to work on. the contents of the textbook are the results of research performed over a period of approximately 36 years—up to 2002. during the following 14 years, over 80 original anatomical papers were published from the lab. the topics we described above in the fourth and fifth stages have not covered them completely.
rhoton医生的研究始于脑表和颅底，聚焦于颅神经、血管和脑池等结构，随后研究了颅底手术中颅骨和脑之间的关系。在生命的最后一段时间，他又开始研究大脑内部的解剖结构，但是由于研究方法上的一些技术性难题而未能成行。
他希冀研究诸如脉络膜前动脉、m1段等的穿支动脉在脑内的分布情况。譬如，以脉络膜前动脉为例，目前已知其发出数支分支动脉为视神经、杏仁核、钩回和大脑脚供血。然而，尚不清楚哪支分支动脉供应哪个脑区。在不久的将来，使用现有的研究方法将问题解决，或者探寻到新的方法之后，必将完成更为详尽的脑内组织和血管的解剖学研究。
dr. rhoton started his studies from the surface of the brain and cranial base, focusing on such structures as cranial nerves, vessels, and cisterns, and continued to study the relationships between the skull and brain for skull base surgery. toward the end of his life, he started to study the anatomy within the brain, but he was unable to complete it because of some technical difficulties in research methods. he strongly hoped to study the intracerebral distribution of perforating arteries, such as those of the anterior choroidal artery and m1 segment. for example, in the case of the anterior choroidal artery, it was already known that the artery had several branches supplying the optic nerve, amygdala, uncus, and cerebral peduncle. however, it was and still is unclear which branches of the artery supply which areas of the brain. in the near future, more detailed anatomical study on intracerebral tissues and vessels should be completed after solving problems with current research methods or finding new methods.
rhoton医生在过去50年中的研究经历表明，伴随新的手术治疗方式和器材的发展，他的研究课题不断地被赋予新的内容。譬如，以海绵窦为例，他反复研究其解剖结构达7遍以上。正如他所说的，“未来，坚持不懈的显微神经外科解剖学研究必将创造更好和更安全的新术式”，“新疗法的可行性……必须依据更为深刻的解剖学领悟进行评估和指导”。显微外科解剖学研究的重要作用在于解决临床上或手术中提出来的问题，或者证实一些新的观点。机器人辅助显微外科已经起步，并将开辟精准手术新领域。机器人手术的发展必定需要更为充分和详尽的显微外科解剖学研究。
as the progress of dr. rhoton’s work over the past 50 years shows, he kept rebuilding his research projects along with the development of new surgical treatment modalities and instruments. in the case of the cavernous sinus, for instance, he studied its anatomy more than 7 times. as he said, “in the future, there will be new, better, and safer procedures that will continue to evolve out of the continued study of microneurosurgical anatomy” and “new therapeutic possibilities … must be evaluated and directed according to an enhanced understanding of the anatomy.” the important role of microsurgical anatomical research is to solve some questions or prove new ideas that are posed clinically or in surgery. robotically assisted microsurgery has started to develop and will open new frontiers of more delicate and accurate surgery. more adequate and detailed studies of the microsurgical anatomy are and will be required as robotic surgery develops.
当年，rhoton医生出于改善患者疗效的初衷，开始了他的显微神经外科解剖学研究。他曾经多次在其讲座的结尾反复告诫我们：“更准确、更轻柔、更安全”。
感谢美国神经外科医师协会（aans）的巨大努力，rhoton医生得以留下他的伟大遗产——“the rhoton collection”，由此神经外科医生们可以很容易地获取和学习他的全部显微神经外科解剖学研究成果。他认为，我们应该创建解剖结构的三维图像，以有助于在手术过程中准确地判断深浅。他希望神经外科医生们更加熟悉显微神经外科解剖学知识，而且期盼在不久的将来所有神经外科医生都能借助他们的台式电脑便捷地搜寻到这些课程，以便在手术前一天的晚上研究和复习他们感兴趣的特定领域。要创造这样一个有效的学习环境，还有非常多的工作需要去做。
dr. rhoton began his work on microneurosurgical anatomy to improve the care of his patients. he told us repeatedly “more accurate, gentle, and safe” in the final message of his presentations. thanks to the great effort by the american association of neurological surgeons (aans), he leaves a great legacy, “the rhoton collection,” so neurosurgeons may easily access and learn from all of his microneurosurgical anatomical studies. he believed that we should build up 3d photography of the anatomy to aid in the accurate understanding of depth during surgical procedures. he hoped that microneurosurgical anatomy would become familiar to many neurosurgeons, and he dreamed that in the near future all neurosurgeons would be able to access the subject easily through their desk computers for study and for review of specific areas of interest the night before surgery. to create such an effectual learning environment, there is still more work to be done.
结论
conclusions
rhoton医生毕生致力于更安全与更精准的外科手术，对于显微神经外科解剖学研究的贡献无与伦比。追随他的脚步，我们应该继续这些研究，以便依据更为深刻的解剖学领悟评估和指导新疗法的可行性。作者需要强调的是，尽管ct和mri（包括3d重建图像）可以详细呈现放射解剖学影像，显微神经外科解剖学仍然是神经外科医生的路图。对于年轻的神经外科医生来说，通过解剖尸头标本获得的解剖学知识在他们的实践中永远是必不可少的重要内容。
with his lifelong commitment to safer and more accurate surgery, dr. rhoton’s contributions to the understanding of microneurosurgical anatomy are unparalleled. following in his footsteps, study should be continued so that new therapeutic possibilities can be evaluated and directed according to an enhanced understanding of the anatomy. the authors would like to emphasize that microneurosurgical anatomy is still the roadmap for neurosurgeons, even though ct scans and mri studies including 3d reconstruction images may show detailed radiological anatomy. anatomical knowledge through dissection of cadaveric specimens will always be needed for young neurosurgeons to obtain vital knowledge that is essential for their practice.
关键词：rhoton，显微外科解剖学，历史回顾，历史
key words rhoton; microsurgical anatomy; historical review; history
原文出处：matsushima t, matsushima, k, kobayashi, s, et al. the microneurosurgical anatomy legacy of albert l. rhoton jr., md: an analysis of transition and evolution over 50 years. j neurosurg, 2018; 129(5): 1331-1341.
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the microneurosurgical anatomy legacy of albert l. rhoton jr., md: an analysis of transition and evolution over 50 years
作为显微神经外科解剖学研究的先驱，albert l. rhoton jr.给这一不断拓展的领域带来的是激动与领悟。
他所做工作的影响已经被公认为神经外科历史上的基石之一，得以促使全球神经外科医生的手术都变得更加安全与微创。
rhoton医生先后率领他的119位研究员和4位医学插画师（bob beach、carla lenkey、david peace和margaret e. “robin” barry）共同发表了大量优秀著作，已经被汇编于教科书《cranial anatomy and surgical approaches》和网站“the rhoton collection”之中。然而，他的研究思想在数十年间的演变过程却并不为世人所熟知。我们作为他曾经的研究员的代表，在本文中基于历史的视角回顾了他的大量著作，并且探讨了显微神经外科解剖学研究的前景。
as a pioneer of the study of microneurosurgical anatomy, albert l. rhoton jr. brought excitement and understanding to this expanding field. the impact of his work has been heralded as one of the cornerstones in the history of neurosurgery that led to safer and gentler surgical treatment by neurosurgeons all over the world. a large number of excellent works published by dr. rhoton, his 119 fellows, and 4 medical illustrators (bob beach, carla lenkey, david peace, and margaret e. “robin” barry) were compiled into the textbook cranial anatomy and surgical approaches and “the rhoton collection” (fig. 1, tables 1 and 2). however, the process by which his research ideas evolved over the years is not well known. in this article, we review his numerous works from a historical perspective, on behalf of all his former research fellows, and discuss future prospects for microneurosurgical anatomical research.
我们复习了过去50年间编撰的大约500种出版物，其中包括了160余篇重要的原创性文章。然后，按照时间顺序将其划分为5个阶段，分别对每个阶段进行解读，并且对第一阶段的划时代研究作了较为详细的论述。此外，《journal of neurosurgery》的部分封面曾经刊发了rhoton医生及其研究员所撰手稿的插图，我们展示了其中一些具有重要历史意义的研究课题的插图以供读者参阅。
we reviewed approximately 500 publications written during the last 50 years, including over 160 major original articles, and then divided them chronologically into 5 stages. each stage is explained individually, and the epoch-making studies of the first stage are discussed in some detail. the front covers of the journal of neurosurgery issues with the figures from the manuscripts written by dr. rhoton and his fellows and some figures representing the features of the historically important projects are shown for visual reference (figs. 2 and 3).
显微神经外科解剖学的萌芽
dawn of microneurosurgical anatomy
和很多先驱一样，rhoton医生在开展研究之初，也是不得不工作在一个极不理想的环境之中。20世纪60年代后期，他在罗切斯特市梅奥医学中心任职的时候，即开始使用猴子进行颅神经的临床解剖学研究。随后，又借助尸检标本的脑和颞骨，重点报道了颅神经变异的详尽解剖。他作此选择的一个原因是颅神经走行于颅底和脑干表面。
as is the case with many pioneers, dr. rhoton had to work in an environment that was far from optimal when he performed his initial research. while a member of the staff at the mayo clinic in rochester in the latter half of the 1960s, he began his anatomical study of the cranial nerves (cns) for clinical purposes using monkeys. then, using autopsy brains and temporal bones, he focused his reporting on the detailed anatomy of the cranial nerves with variations (fig. 3a). one of the reasons for his choice was that the cranial nerves coursed on the surface of the brainstem and skull base.
1972年，rhoton医生移居佛罗里达州盖恩斯维尔市，被聘任为佛罗里达大学外科学系的神经外科主任。1975年，他仰仗数笔慈善捐款建立了theodore gildred显微神经外科实验室，用于开展研究和教学。通过研发与完善人体尸头标本动静脉彩色乳胶灌注系统，以及出自艺术家之手的绘图和经过修描的照片，他借助其出版物建立了一套可视化的和易于理解的显微外科解剖学新标准。
装备精良的实验室也使得他能够更加精细地聚焦于诸如如何更安全地治疗垂体肿瘤和听神经瘤患者等自己感兴趣的手术领域。rhoton医生还热衷于研究同时代世界各地其他神经外科医生的手术技巧，尤其对m. gazi yaargil医生的手术及其所发表的报告印象深刻，而且利用灌注尸头标本从解剖学视角详细审视了这些报告的内容。
in 1972, he moved to gainesville, florida, and was appointed chief of the division of neurosurgery in the department of surgery at the university of florida. in 1975, thanks to several philanthropic contributions, he was able to establish the theodore gildred microneurosurgical laboratory, a facility for both research and education. by developing and refining a system of colored-latex injection of arteries and veins in human cadaveric specimens coupled with artists’ renderings and retouched photos, he set a new standard for visualizing and understanding microsurgical anatomy with his publications. the well-equipped laboratory also allowed him to focus in greater detail on his surgical areas of interest, such as the safer treatment of patients with tumors of the pituitary gland and acoustic neuromas. he was a keen student of the operative techniques of other contemporary neurosurgeons from around the world. he was particularly impressed by the operative and published reports of dr. m. gazi yaargil. utilizing his injected cadaveric specimens, dr. rhoton examined the contents of those reports in great detail from the anatomical point of view.
rhoton医生早期的巨著之一是听神经瘤手术中面神经的研究。在那个时代，此类肿瘤大多数只有在非常巨大的时候才会被发现，手术中经常损伤面神经。他在手术中发现，在解剖学上面神经经常被推移至肿瘤包膜的前半部分；而且先前有病理学家曾经报道过面神经前移。他指出，面神经前移系其大多走行于内听道前上方之故，而肿瘤通常起源于走行在内听道后方的前庭神经。他还建议了手术中探查面神经的两个区域，即内耳道开口处和神经根出脑干区。在这两个区域内，面神经尚未被肿瘤显著推移，神经成分的原始解剖关系很可能保持不变。这项研究有助于听神经瘤手术中保存面神经，引起了其他神经外科医生的关注。
rhoton医生还开展了针对经皮立体定向射频毁损术的三叉神经研究，针对视神经减压术的视神经研究，以及针对舌咽神经痛和颈静脉孔区肿瘤治疗的颈静脉孔和后组颅神经研究。当时彩色幻灯片的制作成本很高，因此研究期间只拍摄了黑白照片。rhoton医生请他的医学插画师对黑白照片进行了润色，帮助读者标清关键结构。经过修描的照片清晰地显示了原始光面照片无法显示的所有重要细节。
one of his great works in the earliest stage was his study of cn vii for acoustic neuroma surgery. in those days, most of these tumors were not found until they were very large, and cn vii was often damaged during surgery. he found anatomically at surgery that cn vii was often stretched over the anterior half of the tumor capsule; its anterior shifting had previously been pointed out by pathologists. he stated that the anterior shift of cn vii was because it mostly coursed in the anterosuperior part of the internal auditory canal, while the tumor usually originated from the vestibular nerves coursing in the posterior part of the canal (fig. 3b). he also suggested 2 regions for finding cn vii intraoperatively, namely, in the lateral end of the internal auditory canal and the nerve’s brainstem exit zone. in these 2 regions, cn vii was not displaced markedly by the tumor, and the original anatomical interrelation of neural components was likely to be maintained. this study benefited the efforts to preserve cn vii during acoustic tumor surgery and attracted the attention of other neurosurgeons. dr. rhoton also studied the trigeminal nerve for the purpose of percutaneous stereotactic radiofrequency lesioning, the optic nerve for optic nerve decompression, and the jugular foramen and the lower cranial nerves for the treatment of glossopharyngeal neuralgia and jugular foramen tumors. at that time, because making color slides was costly, only black-and-white photographs were taken during the research. dr. rhoton asked his medical illustrators to retouch black-and-white photographs to clarify critical structures to help the reader. the retouched prints clearly showed all the important details that the original glossy prints would have failed to display.
自20世纪60年代末开始，垂体肿瘤经蝶手术进展迅速。rhoton医生研究了鞍区和海绵窦的解剖，阐明了蝶鞍前壁鼻中隔附着处和海绵窦间静脉连接等的变异。此外，他还研究了蝶窦外侧壁，确定了颈动脉隆突，并且报道了其厚度和缺如概率。在这些报告中，他汇集并重新整理了经蝶手术所需的解剖学知识，并提供了彩色图解和经过修描的黑白照片。近年来，随着从显微镜到内镜的技术改进，如此而得的解剖学知识对于各种经鼻入路的最新进展作出了巨大贡献。
transsphenoidal surgery for pituitary tumors progressed rapidly starting in the late 1960s. dr. rhoton studied the anatomy of the sellar region and cavernous sinus. he clarified variations of the septal insertion on the anterior floor of the sella turcica and those of the intercavernous venous connections. he furthermore studied the lateral surface of the sphenoid sinus and pointed to the carotid prominence (bulging of the internal carotid artery [ica]), and reported on its thickness and the frequency of its defects. in these reports he accumulated and reorganized the anatomical knowledge necessary for transsphenoidal surgery, providing color illustrations and retouched black-and-white photographs (fig. 3c). the anatomical knowledge thus obtained has contributed greatly to recent advances in various transnasal approaches, as techniques evolved in recent years from microscopic to endoscopic.
与颅内动脉瘤直接夹闭手术的发展同步，rhoton医生于20世纪70年代末还开始了一系列关于动脉及其穿支的研究课题。他首先研究了大脑前-前交通-回返动脉复合体，而且经常会在讲座中提问heubner回返动脉起自哪一部分。其中有关基底动脉上段及其穿支的课题，为难度较大的基底动脉瘤夹闭手术提供了巨大的帮助。另外，该系列研究还拓展至脉络膜前动脉、m1段血管穿支和颈内动脉颅内段及其穿支。关于颈内动脉床突以上的部分，他提出了一种新的分段方法：分别基于眼动脉、后交通动脉和脉络膜前动脉的起始位置，划分为眼动脉段、交通动脉段和脉络膜动脉段。
如果认为有必要使读者更加明了，他会毫不犹豫地重新分类或创建新的命名。他还在该系列研究中最终从3个方面演示了囊性动脉瘤的解剖。这些外科解剖学研究成果给神经外科医生们提供了极大的帮助，先前他们只能通过神经放射科医生撰写的论文和教科书，或者基于血管造影的发现研究动脉及其分支的解剖。在这一系列的研究中，rhoton医生及其研究团队开始使用动脉内注射红色丙烯酸或乳胶的方法，以便于血管分支的解剖。
in accordance with the development of direct clipping for intracranial aneurysms, dr. rhoton also started a series of projects on arteries and their perforators in the late 1970s. he first studied the anterior cerebral–anterior communicating–recurrent artery complex, and in his lectures he often asked which portion the recurrent artery of heubner originated from (fig. 3d). the project on the upper basilar artery and its perforators was of great help for clipping difficult basilar aneurysms. rhoton extended this series to the anterior choroidal artery, perforators from the m1 segment, and the intracranial ica and its perforators. regarding the supraclinoid portion of the ica, he suggested a new segmentation: ophthalmic, communicating, and choroidal segments based on the site of origin of the ophthalmic, posterior communicating, and anterior choroidal arteries, respectively. he did not hesitate to reclassify or coin new names if he thought it necessary for readers to have more clarity. in this series, he finally presented 3 facets of the anatomy of saccular aneurysms. the results of these studies on surgical anatomy enormously benefited neurosurgeons who had previously been able to study the anatomy of the arteries and their branches only through papers and textbooks written by neuroradiologists and based on angiographic findings. for this series, rhoton and his group began using the injection of red-colored acrylic or latex into arteries to facilitate dissection of branches.
20世纪70年代，手术显微镜开始被用于微血管减压术治疗三叉神经痛。当rhoton医生开始关注这一手术的时候，他在显微外科实验室中针对后颅窝，特别是小脑桥脑角内颅神经与动脉血管的解剖关系进行了一系列深入研究。这些研究对于全球神经外科医生更加安全地实施后颅窝手术多有裨益。最初的研究聚焦于小脑上动脉和三叉神经的关系，以及其与三叉神经痛的潜在因果联系。由于当时尚不清楚面神经根出脑干区动脉减压的重要性，因此接下来的研究课题较多地关注于小脑前下动脉-面神经-位听神经复合体的研究。为阐明面肌痉挛的解剖基础，随后又开展了面神经根出脑干区与相关动脉之间关系的研究。
in the 1970s the operative microscope began to be used for the treatment of trigeminal neuralgia via microvascular decompression (mvd). as dr. rhoton began to focus on the operative procedure, he instituted an in-depth series of studies in the microsurgical laboratory of the anatomical relationships between cranial nerves and arteries in the posterior fossa, especially in the cerebellopontine angle. these studies have aided neurosurgeons throughout the world to more safely perform surgery in the posterior fossa. the first study focused on the relationships of the superior cerebellar artery to cn v and its potential causal relationship with trigeminal neuralgia. much attention was paid to the study of the anterior inferior cerebellar artery–cn vii-viii complex in the next project, since the importance of arterial decompression at the exit zone of cn vii was not well known at that time. to clarify the anatomy of hemifacial spasm, the relationships between the exit zone of cn vii and the related arteries were later examined.
为了便于学习和记忆解剖学关系，rhoton医生以制定解剖学“原则”而闻名。通过这些研究，他开始倡导“3原则”，以有助于对后颅窝基本解剖结构，如小脑外表面、脑干、小脑脚、小脑-脑干裂、小脑动脉和静脉的理解。这一原则包括小脑桥脑角内的3组神经血管复合体：其上部的滑车神经、三叉神经及小脑上动脉，中部的面神经、位听神经及小脑前下动脉，下部的后组颅神经和小脑后下动脉。以上3组结构涉及三叉神经痛、面肌痉挛和舌咽神经痛等血管压迫综合征。其中一位作者（t.m.）在微血管减压术中应用“小脑桥脑角3原则”，将枕下外侧入路分为3种：显露三叉神经的外侧幕下小脑上入路、显露面神经根出脑干区的小脑绒球下入路和显露舌咽神经的髁窝入路。
to facilitate learning and retention of anatomical relationships, dr. rhoton was well known for making “rules” of anatomy. through these studies, he started to advocate the “rule of 3” as an aid to understanding the basic anatomy of the posterior fossa, including the cerebellar surfaces, brainstem, cerebellar peduncles, cerebellar-brainstem fissures, cerebellar arteries, and veins. this rule includes 3 neurovascular complex groups in the cerebellopontine angle: cns iv and v and the superior cerebellar artery in the upper portion, cns vii and viii and the anterior inferior cerebellar artery in the middle portion, and the lower cranial nerves and the posterior inferior cerebellar artery in the lower portion. these 3 groups are involved in the vascular compression syndromes trigeminal neuralgia, hemifacial spasm, and glossopharyngeal neuralgia. one of the authors (t.m.) applied the “rule of 3 in the cerebellopontine angle” in his mvd surgeries and divided the lateral suboccipital approach into 3 approaches: the infratentorial lateral supracerebellar approach to the trigeminal nerve, the infrafloccular approach to the exit zone of the facial nerve, and the transcondylar fossa approach to the glossopharyngeal nerve.
rhoton医生引用率最高的5篇论文中的4篇撰写于第一阶段。这些论文的内容在当时是非常新颖的，许多神经外科医生都认为十分重要。
four of dr. rhoton’s 5 most-cited papers were written during the first stage (table 3). the contents of those papers were very new then and considered very important by many neurosurgeons.
服务于普通神经外科学的显微解剖
study of basic microneurosurgical anatomy for general neurosurgery
20世纪80年代，rhoton医生将其研究拓展至其他解剖部位及结构，包括脑室、静脉、枕骨大孔、小脑幕切迹和脑池。
正如他最初设想的那样，这是一个“制图”的过程。在rhoton医生开展研究之前，解剖学家编撰的教科书中主要描述重要神经结构与脑室的关系，几乎没有脑室相关血管的任何表述。
rhoton医生收集了解剖学家所描述的脑室与神经结构和放射科医生所描述的血管结构的信息，并且更多地以其在神经外科手术中的重要性为主线，站在神经外科视角上对其进行了重新整理。
rhoton医生在这些关于脑室的课题中，不仅聚焦于显微外科解剖学，还关注到手术入路。他首先针对第三脑室进行研究，并且在两篇论文中报道了他的研究结果：第一部分涉及显微外科解剖学，第二部分则涉及手术入路。在后续关于第四脑室的研究课题中，最初的显微外科解剖学论文发表之后，他和其中一位作者（t.m.）还曾试图再发表一篇有关手术入路的论文，但是当时除中线经小脑蚓部入路之外并未述及其他入路。
rhoton医生通过标本的分步解剖对第四脑室的背侧显露进行了验证，并且阐明了小脑延髓裂的解剖结构，进而提出了一种全新的革命性手术入路。
目前，这一众所周知的所谓经小脑延髓裂入路或膜髓帆入路的新入路正在被广泛使用。上述两种命名均出自该解剖学研究课题，都是我们在实验室内外经过讨论后确定的。rhoton医生在有关侧脑室的课题中，最为关注脉络膜裂，提出了经由该裂隙的安全入路；随后更为深入地研究了经由脉络膜裂的手术入路，并且进行了单独报道。
in the 1980s, dr. rhoton extended his studies to other anatomical regions and structures, including the ventricles, the veins, the foramen magnum, the tentorial incisura, and the cisterns. this was a “mapmaking” process as he initially envisioned it. prior to dr. rhoton’s studies, the relationships of important neural structures to the ventricles had been primarily described in textbooks written by anatomists. there had been hardly any descriptions of blood vessels related to the ventricles. he collected information on the ventricles and the neural structures described by anatomists and the vascular structures described by radiologists and reorganized them more along the lines of neurosurgical importance and perspective. in these ventricular projects, he focused not only on the microsurgical anatomy but also on surgical approaches. he first studied the third ventricle, reporting his results in 2 papers: part 1 focusing on microsurgical anatomy and part 2 on operative approaches. in the next project, which focused on the fourth ventricle, he and one of the authors (t.m.) also attempted to publish a paper on the operative approaches following an initial paper on microsurgical anatomy, but no approaches other than the midline transvermian approach were described at that time. the step-by-step dissection of the specimen to demonstrate the fourth ventricle from the posterior side, which also revealed the anatomy of the cerebellomedullary fissure, later brought the proposal of a new innovative approach. this new approach is now widely used and well known as the trans–cerebellomedullary fissure approach or the telovelar approach. both names were derived from this anatomical project and through our discussions in and outside the lab. in the lateral ventricle project, much attention was paid to the choroidal fissure, and a safe approach through that fissure was described; a further study on the surgical approach through the choroidal fissure was reported independently.
rhoton医生在研究静脉的早期阶段遭遇了因静脉壁薄易碎而致的技术性难题，但是在完成脑室相关课题的同时，静脉注射适宜技术的创建终获成功。rhoton医生最先选择研究的是后颅窝静脉。当时huang和他的同事们已经通过血管造影检查实现了静脉的完美可视化，并且对各支静脉进行了命名。
在此卓越的放射学研究基础上，rhoton医生调整了后颅窝静脉的命名，以便使其更加符合神经外科专业的理解。新的命名与rhoton医生的“3原则”一致。譬如，huang及其同事所命名的“小脑前中央静脉”被调整为“小脑中脑裂静脉”，“岩上静脉”被调整为“小脑桥脑裂静脉”，huang和wolf所命名的“侧隐窝静脉”被调整为“小脑延髓裂静脉”。紧随后颅窝静脉研究其后，rhoton医生还开展了关于岩上静脉复合体的研究课题。对于幕上静脉，他则将其划分为深部静脉系统和浅部静脉系统。
technical difficulties due to fragility of the thin venous wall were encountered in the early stages of the venous studies. eventually succeeding in establishing proper venous injection techniques while completing projects on the ventricles, dr. rhoton chose the veins of the posterior fossa to be studied first. huang and colleagues had reported excellent visualization of the veins during angiography studies and they had already named each vein. based on their remarkable radiological studies, the naming of the veins of the posterior fossa was reorganized in a way to be more suitable for neurosurgical understanding. the new naming was related to dr. rhoton’s rule of 3. for example, the vein referred to as “the precentral cerebellar vein” by huang and colleagues was changed to “the vein of the cerebellomesencephalic fissure,” the vein named “the superior petrosal vein” by huang et al. to “the vein of the cerebellopontine fissure,” and the vein called “the vein of the lateral recess” by huang and wolf to “the vein of the cerebellomedullary fissure.” the study on the veins of the posterior fossa was later followed by the projects on the superior petrosal venous complex. with regard to supratentorial veins, dr. rhoton grouped them into veins of the deep system and veins of the superficial system.
颅底外科学研究
study for skull base surgery
伴随自20世纪80年代中期至90年代初颅底外科学的发展，为了适应颅底入路的最新进展，rhoton医生再次开展了海绵窦、眶部、颞骨、颈静脉孔和枕骨大孔的研究。在此期间，他开始使用彩色照片和插图呈现各种术式的尸头分步解剖。
为回应20世纪80年代所倡议的处理颈动脉-眼动脉动脉瘤的硬膜内外联合直接入路（所谓的dolenc入路），rhoton医生研究了海绵窦及其邻近区域的各种手术入路。同样，为回应kobayashi等人所发表的关于颈动脉陷窝动脉瘤的报告，他又在研究中发现了“环绕颈内动脉床突段的硬膜环”。伴随经岩骨前/后入路的进展，颞骨也被重新研究，不仅验证手术入路，而且将岩上静脉复合体作为一个相关课题进行研究。
随着枕骨大孔侧方入路，如远外侧入路、极外侧入路、经髁入路和经髁窝入路等的进展，再次开展了枕骨大孔后外侧部分的研究，并且将当时提出的几种改良后外侧入路修订为经髁、髁上和髁旁入路。
颈静脉孔区是最困难的手术显露区域之一，耳鼻喉科医生和神经外科医生均曾针对此区域报道过许多入路，从而导致了一定程度的混乱和一些问题。在颈静脉孔区入路的发展进程中，rhoton实验室先后进行过3次解剖学研究，试图予以澄清。第一次是在1975年，主要局限于颅内一侧；第二次是在1997年，重点聚焦于颞骨内侧面的孔道部分；第三次是在2016年，回顾了已经提出的全部手术入路。
关于眶部则分别研究了经颅入路、侧方入路和眶上裂入路。此外，rhoton医生还针对颅面中部及正中颅底、单侧上颌骨次全切除手术入路和颅骨骨膜瓣的血管解剖结构进行了研究。
as skull base surgery evolved from the mid-1980s to the early 1990s, dr. rhoton again studied the cavernous sinus, orbit, temporal bone, jugular foramen, and foramen magnum for the newly developed skull base approaches. during this period he began to use color photographs and illustrations to present step-by-step cadaveric dissections of the various procedures. in response to the proposal in the 1980s of a combined epi- and subdural direct approach to carotid-ophthalmic aneurysms, the so-called dolenc approach, dr. rhoton studied the various surgical approaches to the cavernous sinus and adjacent regions (fig. 3e). also responding to the report of carotid cave aneurysms by kobayashi et al., he picked up “the dural collars and rings around the clinoidal segment of the ica” for the study. with the development of the anterior and posterior transpetrosal approaches, the temporal bone was again studied. not only were the surgical approaches demonstrated, but also the superior petrosal venous complex was studied as a related project. with the development of the lateral foramen magnum approaches, such as the far-lateral, extreme-lateral, transcondylar, and transcondylar fossa approaches, the posterolateral portion of the foramen magnum was again studied, and several modifications of the posterolateral approach thus far proposed were reorganized as the transcondylar, supracondylar, and paracondylar approaches. the jugular foramen is one of the most difficult regions for surgical access and many approaches to this region were reported by both otolaryngologists and neurosurgeons, which caused some confusion and problems. during the course of the development of the approaches to the jugular foramen, efforts were made to clarify them by anatomically studying them 3 times in the rhoton lab: first, in 1975, mainly on the intracranial side; second, in 1997, on the foraminal portion inside the temporal bone; and third, in 2016, reviewing all the proposed surgical approaches. regarding the orbit, the transcranial approach, the lateral approach, and the superior orbital fissure approach were studied separately. the midface and the midline skull base, the unilateral subtotal maxillectomy approach, and the vascular anatomy of the pericranial flap were also examined.
20世纪90年代末，rhoton医生对于三维成像产生了高度兴趣，认为其有助于更加准确地在颅底手术中判断深浅。在toshiro katsuta博士1993年-1995年做研究员期间，rhoton医生开始尝试在显微神经外科解剖进程中进行立体摄影。1998年，katsuta等在其关于颈静脉孔的文章中首次展示了三维投影图像。早期阶段，三维投影是通过使用经由两台幻灯机投影的两套幻灯片获得的。
进入21世纪后，经由国际研究员的帮助，三维投影在rhoton实验室迅猛发展，已经成为讲授颅底外科领域复杂手术解剖和理解脑内纤维形态的重要工具。2006年，shimizu等发布了详细的经典三维文献。他们使用两台水平式偏光滤镜幻灯机，在同一幅银幕上投射出立体像对，观众通过佩戴三维眼镜即可观看到立体影像。rhoton医生要求他的研究员重行颞骨解剖，以便进行三维展示，并且于2007年发表了全部均为三维图像的《anatomy and surgical approaches of the temporal bone and adjacent areas》，占据了整本《neurosurgery》增刊。2015年，martins等还综述了三维数字投影技术在神经外科教学领域的研究进展。
in the late 1990s, dr. rhoton became keenly interested in 3d imaging, which he believed would aid in more accurate understanding of depth during skull base procedures. during the fellowship of dr. toshiro katsuta from 1993 to 1995, dr. rhoton began to experiment with stereophotography of microneurosurgical dissection. katsuta et al. first presented the 3d projection figures in their article on the jugular foramen in 1998. in the early stage, 3d projection could be obtained by using a double set of slides, projected through 2 slide projectors. in the 2000s, 3d projection rapidly advanced at the rhoton lab with the assistance of international fellows. it became an important tool for teaching the complex anatomy of surgical fields in skull base surgery and for understanding intracerebral fiber topography. in 2006, shimizu et al. reported a detailed classic 3d documentation. two slide projectors with polarizing lens filters of horizontal type for each stereoscopic pair projection and a silver screen were used, and the audience members wore 3d glasses. dr. rhoton asked his fellows to dissect the temporal bone again for a 3d presentation, and it was published as “anatomy and surgical approaches of the temporal bone and adjacent areas” with all figures in 3d, occupying an entire supplemental issue of neurosurgery, in 2007. in 2015, martins et al. summarized the progress of 3d documentation describing 3d digital projection in neurosurgical education.
rhoton医生自1999年从佛罗里达大学神经外科主任的职位上退休以后，研究课题便不再仅局限于他自己的手术，而是涉及神经外科更为广泛的领域。最终，他又将研究选题留给了每一个研究员。
after his retirement from the chairmanship of the department of neurosurgery at the university of florida in 1999, the topics of his research projects became less focused on his own surgeries and were taken from broader fields of neurosurgery. eventually he left the selection of research topics to each fellow.
借助神经纤维解剖的脑内结构研究
study of the internal structure of the brain by fiber dissection technique
rhoton医生已经开始使用纤维解剖技术研究脑的内部结构，以便回应ture及其同事对klingler旧有的纤维解剖方法的改进。从借助纤维解剖技术开展视辐射的三维研究开始，rhoton医生进行了一些包括或不包括弥散张量成像的研究。伴随脑干手术的进展，他的研究又拓展至脑干纤维解剖，特别是安全手术入路区域。随着神经外科的多样化，纤维解剖技术已经用于包括听觉脑干植入和脑深部刺激等在内的众多领域的研究。
dr. rhoton began to study the internal structures of the brain using a fiber dissection technique in response to ture and colleagues’ revitalization of klingler’s old method of fiber dissection. starting with a 3d study of the optic radiation by fiber dissection, several studies were undertaken with or without accompanying diffusion tensor imaging. with the development of brainstem surgery, his studies extended to the anatomy of the brainstem fibers, especially with respect to the safe entry zone. in accordance with the diversification of neurosurgery, the fiber dissection technique has been applied to the study of various fields, including auditory brainstem implantation and deep brain stimulation.
服务于新技术的手术解剖学
surgical anatomy combined with new advanced technologies
截至20世纪末，显微神经外科早已成熟。21世纪初，神经外科治疗进一步多样化。因此，rhoton实验室设计了一些课题以满足新的手术方式的需求。譬如，包括内镜手术在内的微创或无创手术，以及与神经导航系统、血管内介入手术、听觉脑干植入和脑深部刺激等各种技术的协同。部分课题则旨在避免某些手术中发生的并发症。至于内镜手术，不只是经鼻内镜手术，而且针对动脉瘤和小脑桥脑角病变的内镜辅助手术也进行了详尽的解剖学研究。
by the end of the 20th century, microneurosurgery had matured, and in the early 21st century neurosurgical treatment became further diversified. accordingly, in the rhoton lab several projects were created to meet the demands of new surgical modalities, such as less or minimally invasive surgery including endoscopic surgery, collaboration with various technologies including the neuronavigation system, endovascular surgery, auditory brainstem implantation, and deep brain stimulation. some projects were designed to avoid surgical complications during certain surgical procedures. in the case of endoscopic surgery, anatomical studies were made in detail not only for endonasal endoscopic surgery but also for endoscopeassisted surgery for aneurysms and cerebellopontine angle lesions.
rhoton医生接收了来自很多不同国家和专业的研究员，其中包括整形外科医生和耳鼻喉科医生，他们也将各自领域的不同文化和新观念带进了rhoton实验室。rhoton医生为全球神经外科教育领域作出了巨大成绩，在很多国家进行过多次讲座，并且开设过大量实操课程。出于教学的目的，他还凭借rhoton实验室的解剖研究制作了颅底及颅神经的三维互动模型。目前，“the rhoton collection”正在美国神经外科医师协会（aans）的网站上持续更新。
dr. rhoton accepted research fellows from many different countries and disciplines, including a plastic surgeons and otolaryngologists, who brought different cultures and new ideas from their fields to the lab. he made tremendous efforts in the education of neurosurgeons all over the world, giving countless lectures and holding many handson courses in various countries. the 3d interactive model of the skull base and cranial nerves for educational purposes was also made from the anatomical studies in the lab. the rhoton collection is being continuously updated on the american association of neurological surgeons (aans) website.
前景展望
future prospects
很多人可能认为，rhoton医生编写的教科书《cranial anatomy and surgical approaches》出版之时，显微神经外科解剖学研究既已逼近终点。但是，本文作者坚信，未来仍有更多的课题需要研究。教科书中的内容是2002年之前大约36年的研究成果。在接下来的14年里，rhoton实验室又发表了80余篇新颖的解剖学论文，我们在第四和第五阶段所描述的主题中尚未将其全部囊括其中。
many people may have thought that microneurosurgical anatomical study was nearly complete when dr. rhoton’s textbook, cranial anatomy and surgical approaches, was published. the authors believe, however, that there are still many more projects to work on. the contents of the textbook are the results of research performed over a period of approximately 36 years—up to 2002. during the following 14 years, over 80 original anatomical papers were published from the lab. the topics we described above in the fourth and fifth stages have not covered them completely.
rhoton医生的研究始于脑表和颅底，聚焦于颅神经、血管和脑池等结构，随后研究了颅底手术中颅骨和脑之间的关系。在生命的最后一段时间，他又开始研究大脑内部的解剖结构，但是由于研究方法上的一些技术性难题而未能成行。
他希冀研究诸如脉络膜前动脉、m1段等的穿支动脉在脑内的分布情况。譬如，以脉络膜前动脉为例，目前已知其发出数支分支动脉为视神经、杏仁核、钩回和大脑脚供血。然而，尚不清楚哪支分支动脉供应哪个脑区。在不久的将来，使用现有的研究方法将问题解决，或者探寻到新的方法之后，必将完成更为详尽的脑内组织和血管的解剖学研究。
dr. rhoton started his studies from the surface of the brain and cranial base, focusing on such structures as cranial nerves, vessels, and cisterns, and continued to study the relationships between the skull and brain for skull base surgery. toward the end of his life, he started to study the anatomy within the brain, but he was unable to complete it because of some technical difficulties in research methods. he strongly hoped to study the intracerebral distribution of perforating arteries, such as those of the anterior choroidal artery and m1 segment. for example, in the case of the anterior choroidal artery, it was already known that the artery had several branches supplying the optic nerve, amygdala, uncus, and cerebral peduncle. however, it was and still is unclear which branches of the artery supply which areas of the brain. in the near future, more detailed anatomical study on intracerebral tissues and vessels should be completed after solving problems with current research methods or finding new methods.
rhoton医生在过去50年中的研究经历表明，伴随新的手术治疗方式和器材的发展，他的研究课题不断地被赋予新的内容。譬如，以海绵窦为例，他反复研究其解剖结构达7遍以上。正如他所说的，“未来，坚持不懈的显微神经外科解剖学研究必将创造更好和更安全的新术式”，“新疗法的可行性……必须依据更为深刻的解剖学领悟进行评估和指导”。显微外科解剖学研究的重要作用在于解决临床上或手术中提出来的问题，或者证实一些新的观点。机器人辅助显微外科已经起步，并将开辟精准手术新领域。机器人手术的发展必定需要更为充分和详尽的显微外科解剖学研究。
as the progress of dr. rhoton’s work over the past 50 years shows, he kept rebuilding his research projects along with the development of new surgical treatment modalities and instruments. in the case of the cavernous sinus, for instance, he studied its anatomy more than 7 times. as he said, “in the future, there will be new, better, and safer procedures that will continue to evolve out of the continued study of microneurosurgical anatomy” and “new therapeutic possibilities … must be evaluated and directed according to an enhanced understanding of the anatomy.” the important role of microsurgical anatomical research is to solve some questions or prove new ideas that are posed clinically or in surgery. robotically assisted microsurgery has started to develop and will open new frontiers of more delicate and accurate surgery. more adequate and detailed studies of the microsurgical anatomy are and will be required as robotic surgery develops.
当年，rhoton医生出于改善患者疗效的初衷，开始了他的显微神经外科解剖学研究。他曾经多次在其讲座的结尾反复告诫我们：“更准确、更轻柔、更安全”。
感谢美国神经外科医师协会（aans）的巨大努力，rhoton医生得以留下他的伟大遗产——“the rhoton collection”，由此神经外科医生们可以很容易地获取和学习他的全部显微神经外科解剖学研究成果。他认为，我们应该创建解剖结构的三维图像，以有助于在手术过程中准确地判断深浅。他希望神经外科医生们更加熟悉显微神经外科解剖学知识，而且期盼在不久的将来所有神经外科医生都能借助他们的台式电脑便捷地搜寻到这些课程，以便在手术前一天的晚上研究和复习他们感兴趣的特定领域。要创造这样一个有效的学习环境，还有非常多的工作需要去做。
dr. rhoton began his work on microneurosurgical anatomy to improve the care of his patients. he told us repeatedly “more accurate, gentle, and safe” in the final message of his presentations. thanks to the great effort by the american association of neurological surgeons (aans), he leaves a great legacy, “the rhoton collection,” so neurosurgeons may easily access and learn from all of his microneurosurgical anatomical studies. he believed that we should build up 3d photography of the anatomy to aid in the accurate understanding of depth during surgical procedures. he hoped that microneurosurgical anatomy would become familiar to many neurosurgeons, and he dreamed that in the near future all neurosurgeons would be able to access the subject easily through their desk computers for study and for review of specific areas of interest the night before surgery. to create such an effectual learning environment, there is still more work to be done.
结论
conclusions
rhoton医生毕生致力于更安全与更精准的外科手术，对于显微神经外科解剖学研究的贡献无与伦比。追随他的脚步，我们应该继续这些研究，以便依据更为深刻的解剖学领悟评估和指导新疗法的可行性。作者需要强调的是，尽管ct和mri（包括3d重建图像）可以详细呈现放射解剖学影像，显微神经外科解剖学仍然是神经外科医生的路图。对于年轻的神经外科医生来说，通过解剖尸头标本获得的解剖学知识在他们的实践中永远是必不可少的重要内容。
with his lifelong commitment to safer and more accurate surgery, dr. rhoton’s contributions to the understanding of microneurosurgical anatomy are unparalleled. following in his footsteps, study should be continued so that new therapeutic possibilities can be evaluated and directed according to an enhanced understanding of the anatomy. the authors would like to emphasize that microneurosurgical anatomy is still the roadmap for neurosurgeons, even though ct scans and mri studies including 3d reconstruction images may show detailed radiological anatomy. anatomical knowledge through dissection of cadaveric specimens will always be needed for young neurosurgeons to obtain vital knowledge that is essential for their practice.
关键词：rhoton，显微外科解剖学，历史回顾，历史
key words rhoton; microsurgical anatomy; historical review; history
原文出处：matsushima t, matsushima, k, kobayashi, s, et al. the microneurosurgical anatomy legacy of albert l. rhoton jr., md: an analysis of transition and evolution over 50 years. j neurosurg, 2018; 129(5): 1331-1341.
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