Practical neuroanatomy teaching in the 21st century

Manuscript submitted for NeuroGenesis series, Annals of Neurology

Bernard S. Chang1, M.D., M.M.Sc. and Zoltán Molnár2, M.D., D.Phil.

1.

Harvard Medical School, Comprehensive Epilepsy Center, KS-457, Beth Israel

Deaconess Medical Center, 330 Brookline Ave, Boston MA 02215, USA phone (617) 667-2889, fax (617) 667-7919, e-mail [email protected]

2. University

of Oxford, Department of Physiology, Anatomy and Genetics, Le Gros

Clark Building, South Parks Road, Oxford, OX1 3QX, UK e-mail: [email protected]

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1002/ana.24405 This article is protected by copyright. All rights reserved.

Annals of Neurology

Like much else in medical practice, research, and education, the teaching of neuroanatomy is facing changing times. For the two of us, who lead courses for medical students at Harvard in the U.S. and at Oxford in the U.K., teaching neuroanatomy has been a career highlight, and we consider ourselves extremely fortunate to be able to influence the next generation of physicians. For us the job is rewarding, stimulating, and itself educational, but we also recognize a number of growing challenges as we look toward the future. For one, the perception of neuroanatomy from the medical community is often a conflicted one. Professional prizes and distinctions are more commonly awarded for research rather than for high-quality teaching, no matter what the subject, but teaching medical student neuroanatomy in particular can be seen as a thankless task. Both of us have had the experience of introducing ourselves to colleagues as neuroanatomy course leaders, only to be met with what could best be described as a combination of pity and skepticism. Pity, presumably because neuroanatomy is seen as a difficult and unenviable subject to teach, and skepticism, presumably because non-neurologist colleagues are doubtful of its importance in this day and age [1]. Perhaps more troubling, a surprising number of practicing clinical neurologists, when specifically asked, admit that they did not particularly enjoy medical school neuroanatomy – not that the subject matter did not appeal to them, but that their instruction in it left much to be desired. However, both of us have also had the pleasure of meeting former students who are now accomplished clinicians or researchers and hearing accounts of the lasting stimulation and motivation that learning neuroanatomy provided.

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Many of the challenges facing neuroanatomy teachers are generational in nature. The students are different, the technology is different, the available time and resources are different, and the faculty members are different. And while the subject matter would appear to be the same, in fact the aspects of it that are deemed the most fundamental and most relevant to clinical practice do change over time, as our understanding of human neurological disease advances, our ability to visualize anatomical lesions through imaging increases, and our capacity to tailor individual treatments for patients expands. In our opinion, however, the beauty of the nervous system, the logic of (most of) its pathways, and the possibility (indeed, necessity) of clinico-anatomical correlation in proper diagnosis combine for a subject that in some ways is an ideal one for preclinical students. After all, even the most inexperienced novice can localize from first principles if familiar with the symptoms, examination findings, and relevant functional anatomy of a case in enough detail. How much more exciting it is for a student to realize that learning neuroanatomy allows her to truly “figure out” a case from scratch, rather than be told that it will take 40 more years of experience before she can recognize such-and-such a disease correctly. Moreover, considerable time and expense can be saved by establishing and narrowing down the differential diagnosis based on neuroanatomical principles, an important factor in this cost-conscious age. During a recent sabbatical visit, we started comparing neuroanatomical teaching between Harvard and Oxford. In both cases, practical laboratory sessions are integral parts of a larger course. At Oxford, neuroanatomy is taught as part of a

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medical neuroscience course given to undergraduates pursuing careers in clinical medicine; the course presents basic science, including an understanding of neural cell biology and neuronal function, as well as neuroanatomy and physiology at a systems level, and the important clinical disciplines of neuroimaging, clinical neurology, psychiatry and psychology. Links from molecule to cell to system, and between function and dysfunction, are critical. At Harvard, students in the integrated neurology/neuroscience course are usually at least four years older than their Oxford counterparts, having completed their bachelor’s degree (and often one or more additional years of research or other experience) before matriculating at medical or dental school. The Harvard course presents the most clinically relevant basic neuroscience, followed by a more detailed problem-based approach to nervous system disease states, including topics such as pathophysiology and treatment. In spite of these notable differences (Table), we find a number of surprising commonalities across our two systems and share three fundamental goals in teaching our students: (1) To instill in all future physicians the basic level of understanding of nervous system anatomy we believe to be necessary to approach patients with neurological complaints. (2) To inspire and excite the smaller subset of students who might potentially be inclined to consider clinical specialization in a neuroscience-related field, who will undoubtedly return to the material to expand their knowledge over what might turn out to be a lifetime’s worth of study.

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(3) To motivate students at an early stage to turn their attention to neuroscience research and consider combining clinical and research careers in whatever field they choose. In this spirit, we offer our own reflections on some key questions faced by neuroanatomy teachers today. Many of these issues are also relevant to other aspects of the preclinical curriculum, such as gross human anatomy, while others are more specific to the nervous system. While we have our own opinions on these topics, there are no exclusively correct answers, and we hope that this article will engender a lively discussion that will help us and others to take our “thankless task” and make it even more rewarding for teachers and students alike in the future.

Who should teach neuroanatomy? The seemingly obvious answer to this question is, of course, “neuroanatomists.” But what exactly is a neuroanatomist these days? One would be hard-pressed at most medical schools to find faculty members purely devoted to the characterization of nervous system structure. Instead, among laboratory-based faculty we typically have neurobiologists of various persuasions, including developmental neurobiologists, systems neuroscientists, basic neurophysiologists, neurogeneticists, and neuropharmacologists. Among clinical faculty we have neurologists of various subspecialties, neuroradiologists, neurosurgeons, neuropathologists, and psychiatrists. All of these individuals are familiar with neuroanatomy at some scale and level of complexity.

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At some schools, neurobiologists who are familiar with human neuroanatomy are responsible for teaching preclinical medical students, but they may find it harder to give fresh examples of clinical cases that invoke the need for such neuroanatomical knowledge in practice. Clinical neurologists, meanwhile, can provide anecdotes galore but may be less comfortable navigating histological anatomy and specimen dissection and are often less familiar with molecular mechanisms and more current basic research directions. Neuropathologists play large roles in many schools’ curricula, and neuroradiologists are often closely involved as well. With a trend toward consolidating preclinical teaching into the hands of a smaller number of core faculty, rather than a large number of rotating experts, it becomes even more critical to think hard about who should hold the reins of neuroanatomy teaching. It is our own opinion that suitable neuroanatomy faculty can come from any of the above fields, and we have seen superb teachers from all of these backgrounds. In the Harvard course, which is more directly clinically oriented and includes students who have more advanced science backgrounds, active clinicians are often prized. At Oxford, a combined team of both clinicians and basic researchers is considered the most effective. In either case, a mastery of neuroanatomy appears to be a sine qua non, since the subject is disproportionately intimidating to students [2] and they rely upon an expert to guide them through the material. Perhaps the most important attribute of a successful neuroanatomy teacher, however, as in so many fields, is simply the degree of dedication and enthusiasm.

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What neuroanatomy should we teach? There is a temptation to answer glibly, “Why, all of it, of course.” Yet even the most hardened old-school veteran would acknowledge that this would be impossible, and perhaps undesirable even if possible, since it would take focus away from the most critically important subset of neuroanatomical knowledge students must know. Sir Arthur Conan Doyle, through Sherlock Holmes’s voice in A Study in Scarlet, likened the brain to a finite physical space, saying that “there comes a time when for every addition of knowledge you forget something that you knew before. It is of the highest importance, therefore, not to have useless facts elbowing out the useful ones.” While cognitive neuroscientists might disagree with the construct, the idea holds familiar appeal. But how do we decide what the core, fundamental subset of knowledge is? Senior clinicians are always suspicious that less and less neuroscience is being taught before students arrive on the wards. All we can say is that this is absolutely true. There are many reasons for this, including the need to teach important subjects that were not as well-developed (genetics, genomics) or were simply ignored (nutrition) in decades past, and a recognition of the value of exposing students to the clinical approach earlier in the undergraduate medical curriculum. Fundamentally, though, in an age in which factual information is available within seconds on a handheld device, the value of memorizing large volumes of neuroanatomy so that it is (theoretically) readily accessible for a patient encounter seems to pale in comparison to the importance of understanding the conceptual framework of nervous system pathways. We all know trainees who can recite

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esoteric names and circuits ad nauseam but have difficulty applying their knowledge to patients. As both of us have purposefully decreased the amount of obscure detail that is taught (and tested) by concentrating on a core curriculum in our courses over the years, there appears to have been a welcome increase in the amount of retained information concerning the fundamental pathways once students enter the clinical rotations. While most of what is taught is still forgotten and must be relearned as needed, the subset that is readily recalled seems to align more with the most important material, when less detail is presented in the first place. At the same time, however, there are topics that become overtly incomplete and lacking in context if reduced to an extreme (e.g., teaching only the “most important” of the 12 cranial nerves leaves unexplainable and unacceptable gaps in an appreciation of these structures). Part of the difficulty faced in our courses is the presence of external entities that impart their own views on what body of neuroanatomy is most relevant to learn, at least for testing and licensing purposes. In Oxford, teaching follows a curriculum document that is regularly revised by the members of the Neuroscience Course Committee, with an overall framework regulated by the General Medical Board of the U.K. The course committee contains both basic researchers and active clinicians and receives regular feedback from internal and external examiners. At Harvard, the course aims primarily to prepare students for their subsequent clinical clerkship in neurology, and the content and assessments are frequently revised in accordance with what is seen as most clinically fundamental. However, Harvard

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students can face competing demands when faculty emphasize core principles of functional localization, for example, while U.S. national medical licensing bodies focus on classic “buzzwords” and traditionally tested minutiae in their standardized board examinations.

How should we teach neuroanatomy? A neuroanatomy faculty member from 50 years ago would find a medical school teaching laboratory in 2015 both familiar and unfamiliar. While brain and spinal cord specimens are still laid out carefully, ready for small groups of students to inspect and dissect, at both Harvard and Oxford the available specimens are inferior in number and quality to what used to be available, and much less hands-on time is spent with them. While students still use atlases open to photographic images and review glass slides (or “virtual” microscopic images) of stained sections, they also arrive bearing laptops, tablets, and smartphones, can call up images and explanations of structures and pathways with ease, and can share their findings with each other in a peer-to-peer teaching style that has always been a hallmark of an excellent learning environment [3]. Outside the teaching laboratory, students can prepare or review by watching bite-sized videos, study sections and plastinated specimens in two- and three-dimensional scans, and test their knowledge on quizzes of their own or their instructors’ creation. For an interesting historical comparison, the reader is referred to the cases used for teaching by Sir Charles Sherrington and Sir Wilfrid Le Gros Clark (former heads of the University Laboratory of Physiology and Department of Human Anatomy at Oxford,

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respectively), which have now been made available (https://history.medsci.ox.ac.uk/slides/)[4]. The question reasonably arises as to how neuroanatomy teaching should change to best meet the needs of this generation of students. Indeed, some schools no longer use hands-on brain dissection at all, and instead rely on prosections and images. Many preclinical medical students may never encounter brain-cutting again in their careers – does that mean we should emphasize specimen learning in their one chance to be exposed to it in detail, or should we shift to teaching more from radiological images, which they will undoubtedly see in the future? Students going into a neuroscience-related field will have opportunities to revisit brain-cutting, of course, but perhaps fewer would be inspired to go into those fields without exposure to the “real thing” early on. Should the focus be on small-group and teambased exercises in clinico-anatomical localization, getting right to the heart of how this knowledge will be used on the wards, or is there something lost if students do not work their way through dissections? Three commonly used pedagogical methods in neuroanatomy, namely hands-on dissection, problem-based learning, and computer-assisted learning, each have their own advantages and disadvantages. Dissection/inspection allows students to learn anatomy in detail, including normal variations, and takes advantage of fully exposed structures, but interacting with real specimens may not have as much affective valence for students as it once did. Dissection is probably the most time- and labor-intensive of the usual pedagogical methods, and it is increasingly difficult to obtain high-quality human specimens as cadaveric

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donations and hospital postmortem examinations continue to decline. At Harvard there are still dedicated human brain-cutting exercises, but at Oxford sheep brains and deer eyeballs are used now to provide dissection opportunities to all students. Problem-based learning, as its name suggests, focuses on solving realistic clinical cases rather than rote memorization [5]. With instant access to factual information at students’ fingertips these days, there is the opportunity to emphasize the value of patience in the struggle to understand difficult concepts. At Oxford, a traditional weekly tutorial structure provides a superb opportunity to use problembased learning to teach critical thinking. At Harvard, similar methods are used extensively in the broader integrated neurology/neuroscience course but clinical problem-solving is also taught in the neuroanatomy lab sessions, with specimens, images, and clinically trained instructors all at close hand. Computer-assisted learning, meanwhile, provides a wealth of teaching material to students to work through at their own pace: three-dimensional brain scans, photographs of dissected specimens, high-resolution histological images, and even explanatory videos [6-8]. While it is difficult to imagine a successful neuroanatomy course that does not incorporate digitally available resources these days, an excessive focus on such methods may deprive students of that all-important personal connection to faculty members [9]. In our opinion, all of these pedagogical methods should be employed in various settings and at various times in teaching neuroanatomy, since they are complementary and reinforce each other.

Neuroanatomy teaching as a sustainable investment

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Medical students are seekers of information. While faculty members used to be seen as expert repositories of knowledge, in more contemporary times they are perhaps best characterized as guides and facilitators to the access and understanding of knowledge. The student, to a large extent, relies on the wisdom and expertise of the teacher to decide what knowledge is most clinically relevant, what the most efficient way to go about learning that knowledge is, and how one can best implement such knowledge in a clinical setting. For neuroanatomy teaching to remain vibrant, there needs to be both recognition of outstanding teachers and formal training opportunities for the next generation of educators. Participation in institutional academies of medical educators, completion of master’s degree or certificate programs in medical education, and competition for research funding in innovative teaching methods can all be potential steps toward establishing education as an element of one’s career at an academic medical center [10]. Promotion pathways focused on preclinical and clinical student education may help to support and sustain those younger faculty who wish to engage in teaching at the very time when a high level of research output and grant income is expected of them. From an institutional point of view, there may be programmatic and even revenue-generating opportunities as well. At Oxford, specialized courses developed in collaboration with other fields can make use of the neuroanatomy practical laboratory curriculum, resources, and facilities. There are close partnerships with radiology, trauma, the Royal College of Surgeons, and the Anatomical Society of Great Britain and Ireland for teacher recruitment and curriculum design, and a

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Diploma in Anatomy Teaching is now provided by a national center in the U.K. Harvard now offers a master’s degree program in medical education as a joint initiative of the medical school and the graduate school of education, and an online open curriculum in gross human anatomy is being developed. Perhaps medical schools around the world could establish international rotating residential courses for young faculty to help them learn the basics, thus improving the caliber of neuroanatomy teaching beyond any one institution’s walls.

Lessons Medicine is ever-changing, and the teaching of neuroanatomy is no exception. It is important to recognize that medical student populations are more heterogeneous and learning preferences more diverse than they used to be [11]. We have spent most of this article focusing on some of the very practical issues faced by us as we attempt to keep our respective courses as current as possible. In our opinion, we must use a variety of different teaching methods: some of the triedand-true experiences such as cadaveric and specimen dissection, but also more flexible exercises that involve problem-based learning and digitally available materials. We both believe, however, that the single most important factor in determining the quality of the medical student experience is the quality of the faculty directly engaged in teaching. It follows, then, that neuroanatomy teaching is most successful when faculty who are good at teaching and want to teach are identified, encouraged, and supported. In this way, we can ensure that future generations of physicians all have a ground floor of nervous system knowledge set

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securely in place early on, no matter how many additional stories of neuroanatomy may need to be constructed in their career.

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Acknowledgements: We thank our students, whose subsequent careers represent the ultimate outcome measure in neuroanatomy education. We are grateful to several colleagues (Ray Guillery, Jeremy Taylor, Alexander Eastwood, and David Cardozo) for their constructive criticisms on an earlier version of this manuscript.

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Table

Student background

Time spent in neuroanatomy practical sessions Pedagogical methods used

Harvard

Oxford

Second-year postbaccalaureate medical students; average age 24 Twelve 2.5-hour sessions

Second-year undergraduate students; average age 19 Ten 3-hour sessions (1.5 hours wet lab and 1.5 hours computer-based activities) Lectures

Wet lab: human brain and spinal cord dissection Computer-based activities and mini-lectures: clinical cases, collections of gross and microscopic images, interactive exercises and presentations

Wet lab: human brain specimen inspection, sheep brain specimen dissection, plastinated materials, models, CT and MRI images Computer-based activities: interactive questions, clinical cases, videos, 3D scans, models

Faculty

For 170 students, about 16 total instructors (onethird senior faculty and two-thirds neurology and neurosurgery house officers, all clinicians).

Neuroanatomy content covered/emphasized

Functionally relevant pathways and major principles. Memorization and nomenclature are deemphasized.

Tutorials For 75 students, 2-4 faculty present with 2-6 additional demonstrators (some clinically qualified, some expert in neuroembryology and histology). Functional and theoretical aspects. Clinical illustrations are provided for better understanding.

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Other elements of the broader neuroscience course

Lectures: 4-5 per week for 7 weeks delivered by basic researchers and clinical specialists Tutorials: 3 per week for 7 weeks of small-group problem-based learning exercises focused on one major neurological disease each week

Assessment

Neuroanatomy quizzes: multiple choice imagebased clinic-anatomical questions. Final exam: short essay questions in response to clinical vignettes drawn from actual neurology ward cases. Tutorial PBL participation

Lectures: 2-3 per week for eight weeks delivered by basic researchers, specialists, and clinicians in synchrony with the practical and clinical demonstrations

Part A: Core curriculum is tested in multiple choice / computer-based exam. This has a strong component in neuroanatomy, but it includes all aspects of neuroscience. Part B: Grades are given based on three essay questions answered on complex topics of neuroscience.

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References: 1. McCarron MO, Stevenson M, Loftus AM, McKeown P. (2014) Neurophobia among general practice trainees: the evidence, perceived causes and solutions. Clin Neurol Neurosurg. 122:124-8. 2. Schon F, Hart P, Fernandez C. Is clinical neurology really so difficult? J Neurol Neurosurg Psychiatry 2002;72:557-9. 3. Hall S, Stephens J, Andrade T, Davids J, Powell M, Border S. Perceptions of junior doctors and undergraduate medical students as anatomy teachers: Investigating distance along the near-peer teaching spectrum. Anat Sci Educ. 2014 MayJun;7(3):242-7. 4. Molnár Z, Brown RE. Insights into the life and work of Sir Charles Sherrington. Nat Rev Neurosci. 2010; 11(6):429-36. 5. Greenwald RR, Ouitadamo IJ. A Mind of Their Own: Using Inquiry-based Teaching to Build Critical Thinking Skills and Intellectual Engagement in an Undergraduate Neuroanatomy Course. J Undergrad Neurosci Educ. 2014 Mar 15;12(2):A100-6. 6. Li Q, Ran X, Zhang S, Tan L, Qiu M. A digital interactive human brain atlas based on Chinese visible human datasets for anatomy teaching. J Craniofac Surg. 2014 Jan;25(1):303-7. 7. Nowinski WL, Chua BC. Bridging neuroanatomy, neuroradiology and neurology: three-dimensional interactive atlas of neurological disorders. Neuroradiol J. 2013 Jun;26(3):252-62. 8. Pani JR, Chariker JH, Naaz F. Computer-based learning: interleaving whole and sectional representation of neuroanatomy. Anat Sci Educ. 2013 Jan-Feb;6(1):11-8. 9. Whillier S, Lystad RP. The effect of face-to-face teaching on student knowledge and satisfaction in an undergraduate neuroanatomy course. Anat Sci Educ. 2013 JulAug;6(4):239-45. 10. Gelb DJ. Advice for clinician educators. Ann Neurol 2014;75:625-30. 11. Svirko E, Mellanby J. Attitudes to e-learning, learning style and achievement in learning neuroanatomy by medical students. Med Teach. 2008;30(9-10):e219-27.

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Practical neuroanatomy teaching in the 21st century.

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