The Growth of American N euro--ophthalmology in the 20th Century

H. Stanley Thompson, MD

Ask almost any American neuro-ophthalmologist this question, "Who was the founder of your subspecialty?" The first name you'll hear is Frank Walsh. There is no doubt that Walsh's 1947 book drew a lot of attention to neuro-ophthalmology, but the kind of clinical problems that a neuro-ophthalmologist faces today have, of course, always been there and they have been addressed by others in the past. As you might expect, American neuro-oph­thalmology stood on the shoulders of European neurol­ogists and ophthalmologists of the late 19th century: in Germany, Westphal, Wernicke, Oppenheim, Uhthoff, and Wilbrand; in France, Charcot, Babinski, and Dejerine; and in England, Jonathan Hutchinson, Hughlings Jack­son, Brudenell Carter, Clifford Albutt, and William Gow­ers. AU were heavily dependent on the neuro-anatomists who had preceded them. Helmholtz's had invented his Augenspiegel in 1851, and suddenly, for the first time, the doctor was able to see the patient's retina. This new technology made ophthalmology a very popular medical specialty, and at the front of the first wave was the aston­ishing young genius, Albrecht von Graefe.

In America, the Civil War gave an unexpected boost to neuro-ophthalmology. There were some Philadelphians in the Medical Corps who knew each other and had a common interest in neurology and ophthalmology. Silas Weir Mitchell (1829-1914) later became famous as a neurologist and novelist, but during the war, he gathered information about injuries to peripheral nerves that later led to important publications with GR Morehouse and WW Keen. In 1864, they carefully described a soldier, shot in the neck at Chancellors ville, who had a condition that was later to be known as Horner syndrome. Keen was to become a renowned surgeon and editor. William Thomson and William Fisher Norris worked together to use photography as a means of recording the appearance of wounds and various pathologic conditions and made

From the Department of Ophthalmology, University oflowa, Iowa City.

Reprint requests to H. Stanley Thompson, MD, Department of Oph­thalmology, University oflowa, Iowa City, IA 52242.

some pioneering contributions to photomicroscopy. These studies in optics no doubt stirred an interest in eye diseases in both of these young men. Norris became the Professor of Ophthalmology at the University of Pennsylvania and the Dean of American ophthalmologists, and William Thomson became a well-known practicing ophthalmol­ogist and teacher at the Wills Eye Hospital.

In 1865, at the end of the Civil War, Norris was dis­charged from the Medical Corps at age 26 and decided to take up the specialty of ophthalmology. His father, an eminent Philadelphia surgeon, had some reservations about these plans, believing that anyone who advertised himself as a specialist was probably a charlatan and a quack. In those years, every would-be ophthalmologist in America wanted to go to Europe to learn about the eye and to pick up enough German to read the ophthalmic literature, so Norris went to Vienna and spent 5 years with Arlt, Jaeger, and Mauthner-a very thorough ophthalmic training. When Norris came back to Phila­delphia in 1870, he attached himself to the University of Pennsylvania as an instructor, and 6 years later, he was the professor of Ophthalmology (Fig 1).

He gathered around him a number of students who later made significant contributions. Among them were Samuel D. Risley (1845-1916), remembered for his rotary prism, George deSchweinitz (1858-1938), who was to be­come Norris's successor at University of Pennsylvania and who was enthusiastic about medical ophthalmology, and Charles A. Oliver, who was to be Norris's co-author on more than one book (Fig 2).

Norris and Oliver prepared a one-volume Text-Book o/Ophthalmology (1893, Lea Brothers, Phila.), which was so exceedingly popular that it was even translated into Chinese. They then undertook to edit a four-volume compendium called "A System of Diseases of the Eye" (1897-1900, J.B. Lippincott, Phila.). It contained many illustrious contributions, including a 200-page chapter by Herman Wilbrand on perimetry that put the analysis of visual field defects due to lesions of the visual pathways onto a firm anatomic footing. Wilbrand strongly rec­ommended that visual fields be done under controlled

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Figure 1. William Fisher Norris (1839-1901).

conditions with great care and with different sizes of test objects. This four-volume set was looked on as an Amer­ican version of the famous Graefe-Saemisch H andbuch der Gesamten Augenheilkunde. Dr. Norris gave great im­portance to the nonsurgical parts of Ophthalmology: he wrote a chapter on "Medical Ophthalmology" for the Pepper System of Medicine.

Herman Wilbrand (1851-1935), the German ophthal­mologist who had made such an important contribution to the success of Norris and Oliver's four-volume, multi­authored work, started in 1899 on a set of his own in collaboration with Alfred Saenger, The Neurology o/the Eye: A Handbook/or Neurologists and Ophthalmologists. There were to be nine volumes in this set. They were published over a considerable time period and were not completed until 1922. These volumes offered a detailed summary of the contributions of German ophthalmology and neurology over the last half of the 19th century, a lot

Figure 2. Charles A. Oliver (1853-1911).

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Figure 3. William Thomson (1833-1907).

of it uncritically assembled, simply so that it would be retrievable.

William Thomson (Fig 3) stayed in the Army until 1868. He was one of the first Philadelphia doctors to limit his practice to diseases of the eye. He was elected to the American Ophthalmological Society in 1870. He was a +5 D hyperope and, as a young man, he had learned that he could read more comfortably if he held a candle flame between his face and the book. Presumably this extra light contracted his pupils and increased his depth offield. Dr. William McClure at the Wills Eye Hospital atropinized Thomson's eyes and gave him his first pair of adequate glasses. This convinced Thomson to become an ophthal­mologist and established a lifelong interest in careful re­fraction, including cycloplegia and full correction of both sphere and cylinder. Weir Mitchell, encouraged by Wil­liam Thomson, liked to emphasize the importance of a good refraction in the management of headaches. As a result of his work as Ophthalmic Surgeon to the Penn­sylvania Rail Road, Thomson developed an interest in color vision problems. His color stick test was an improved version of the Holmgren Wool test for use in color vision testing. In 1872, he became attending surgeon at Wills Eye Hospital and eventually ran a clinic for nonsurgical ophthalmology at Wills Eye Hospital.

When William Thomson retired from his clinic at the Wills Eye Hospital in January 1902, he was succeeded in June by William Campbell Posey (Fig 4), a man who had an even stronger interest in the neurologic problems of vision. Posey collaborated with William Gibson Spiller (Fig 5), the neurologist at the Pennsylvania Hospital, who had spent 4 years in Europe training with Oppenheim, Obersteiner, Edinger, Dejerine, and Gowers. In 1906, they produced a fat, multi-authored textbook, The Eye and Nervous System. There were 100 pages on eye movements by Alexander Duane, 40 pages on the fifth, seventh, and sympathetic nerves by Edward Jackson, and 80 pages on

Thompson . Neuro-ophthalmology in the 20th Century

Figure 4. William C. Posey (1866-1934).

neuroses and psychoses by DeSchweinitz. This was the first American textbook limited to the subject that is now called neuro-ophthalmology, and for a generation, it was the best text on the subject. This book, like Norris and Oliver's, was published by JB Lippincott and was seen as America's answer to Wilbrand and Saenger's series.

At the end of the 19th century, neurology and oph­thalmology were well-established medical specialties, but there were no American neurologists or ophthalmologists who would allow themselves to be referred to as neuro­ophthalmologists. First, they had been trained in one spe­cialty or the other and had no intention of giving it up, and second, the territory of neuro-ophthalmology seemed too ludicrously small. Who would want to devote an entire career to a handful of cranial nerves, the visual pathways through the brain, and one or two mysterious pupillary signs? Just as neurology was part of medicine, so too was neuro-ophthalmology part of medical ophthalmology.

Nonsurgical or medical ophthalmology was a recog­nized subdivision of ophthalmic practice. For example, in An International System of Ophthalmic Practice (1918, P. Blakiston's Son & Co, Phila.), a set of monographs edited by Walter Pyle, there was a volume by Arnold Knapp, Medical Ophthalmology, and R. Foster Moore, a London ophthalmologist, had a popular book, Medical Ophthalmology, and more recent, a book of the same title was produced by F. Clifford Rose.

In 1910, Casey Wood came out with his incredible American Encyclopedia and Dictionary of Ophthalmology, in which some fascinating material has lain buried for 85 years: there is, for example, a 244-page monograph on "The Pupil in Health and Disease" by Derrick T. Vail, Sr., and a 255-page monograph on "Refraction and Ac­commodation" by AE Davis, both in volume 14. This set served to emphasize the enormous amount of knowledge that had to be absorbed to become a good ophthalmol­ogist.

Harvey W. Cushing (1869-1939) put neurosurgery on the map in 1911 with his monograph called "Surgery of

Figure 5. William C. Spiller (1863-1940).

the Head" in volume 3 of Surgery, WW Keen's six-volume text. At about this time, Cushing had been working on pituitary tumors, and he began to place great emphasis on visual field defects as an indication of the location of a brain tumor. Cushing encouraged Clifford B. Walker to do research in perimetry to produce high-quality, trust­worthy visual field mapping in certain neurosurgery pa­tients. Walker later practiced ophthalmology in Los An­geles. During World War I, Cushing was a very busy neu­rosurgeon trying desperately to save a few lives among all the soldiers with shrapnel injuries to the brain, and it fell to the neurologist Gordon Holmes, also working in dif­ficult conditions near the front lines, to sort out the exact representation of the retina in the visual pathways and cortex. On the German side, Wilhelm Uhthoffwas making similar observations. Both Uhthoff and Holmes appar­ently were following up on the work published by Tatsuji Inoue in 1909, based on the casualties of the Russo-Jap­anese war of 1904-1905.

In the first quarter of the century, the tangent screen, as recommended by Bjerrum and R0nne in Copenhagen, was being popularized in America by Alexander Duane, Harry Friedenwald, and Luther C. Peter, and it was be­ginning to replace the arc perimeter. Harry Moss Traquair of Edinburgh, Scotland, following in the footsteps of AHH Sinclair, took a special interest in tangent screen campi­metry, and in 1927, produced a book, An Introduction to Clinical Perimetry, that went through many editions. It was the standard perimetry text until edged out by David O. Harrington's textbook Visual Fields in the late 1950s.

The First Modem Neuro .. ophthalmologists

In 1940, it was possible to count on one's fingers the American ophthalmologists who were taking a special in­terest in visual problems of neurologic origin. They were Lillie, Rucker, Cogan, Leinfelder, Lyle, Kestenbaum, and

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Walsh and not one of them called himself a neuro­ophthalmologist. That was altogether too fancy a word; in fact, the word was seen as an awkward neologism: "Why not ophthalmo-neurologist?" people said.

Gradually, there began to appear at various places in America, specialists who took a particular interest in the area of neuro-ophthalmology. One of the earliest was at the Mayo Clinic. In 1918, Dr. William Benedict had been asked to start a section of ophthalmology there, and he hired a young man named Walter Ivan Lillie. Lillie un­dertook to do the graduate course in ophthalmology at the Mayo Clinic with a minor in neurology. He started working for Dr. Benedict doing the parts of ophthalmology that Dr. Benedict preferred not to deal with: refraction, children, and general medical and neurologic consulta­tions. Later, A very Prangen was hired and began concen­trating on the refraction and motility problems. Then, Henry P. Wagener undertook to do the consultations from internal medicine. This left Lillie with neurologic con-

sultations, chiefly from the neurology and neurosurgery departments within the hospital and a few outside refer­rals. These he did during the day, and in the evening, he did visual fields. He became a staff consultant in 1921 and left Minnesota in 1933 to become the Chairman of Ophthalmology at Temple University in Philadelphia. Lillie published 20 articles on neuro-ophthalmic subjects. C. Wilbur Rucker, who had started an ophthalmic practice in the Twin Cities, then was hired to cover the neurologic consultations. To this team were added Robert Hollen­horst and later Thomas Kearns and James C. Trautmann. This group continued to publish actively in neuro-oph­thalmology through the 1960s (Fig 6).

Meanwhile, PJ Leinfelder (Fig 7) in the next state to the south, at the University of Iowa in Iowa City, clearly was interested in neuro-ophthalmology. Leinfelder was from Wisconsin and trained with CS O'Brien in Iowa City. In 1932, he started as an assistant professor at a salary of $6000 a year. He was to teach general ophthal-

Figure 6. Neuro-ophthalmologists at the Mayo Clinic. Top, Walter Ivan Lillie (1891-1950), Henry P. Wagener (1890-1961), C. Wilbur Rucker (1904-1986); Bottom, Robert Hollenhorst, Thomas Kearns, and James C. Trautman.

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Thompson . Neuro-ophthalmology in the 20th Century

Figure 7. P. ]. Leinfelder (1905- 1988).

mology and ophthalmic surgery, but it was understood that neuro-ophthalmic problems would be thrown his way. His AOS thesis (1938) was about optic atrophy after tract lesions, and for a number of years, he gave a course at the Academy on "The Swollen Disc" and lectured to local ophthalmology groups on neuro-ophthalmic topics. In 1938, O'Brien asked Leinfelder to head a neuro-oph­thalmology section in the department. He was available to the residents and to the surrounding medical com­munity for consultation on neuro-ophthalmic questions until he retired in 1978. Despite all this, Leinfelder always thought of himself as a general ophthalmologist with an interest in neuro-ophthalmology. He never referred to himself as a neuro-ophthalmologist. He would go out of his way to avoid the label. Perhaps this was because he

Figure 8. David G. Cogan at the Verhoeff Society.

also did general ophthalmology and did not want anyone to jump to the conclusion that he was limiting his practice to neuro-ophthalmology. Thompson was hired in 1967 as a full-time neuro-ophthalmologist and was given the chance to pursue his interest in clinical pupillary problems, an interest he had picked up from Lowenstein and Loew­enfeld in 1962.

During the late 1930s, David G. Cogan (1908-1994) (Fig 8) in Boston was pursuing his own interest in neuro­ophthalmology, and in England, an ophthalmologist named R. Lindsay Rea in London put together the lectures that he had been giving on neuro-ophthalmic topics into a substantial text and entitled it simply "Neuro-ophthal­mology." This was 1938 and it was, I believe, the first book on the subject ever to have the word neuro-oph­thalmology on the spine. It was published in America by CV Mosby in St. Louis and came out in a second edition in 1941. Cogan's book, The Neurology of the Ocular Mus­cles, appeared late in 1945. This book was fully referenced,

Figure 9. Donald]. Lyle (1895-1986) and his textbook.

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Figure 10. Alfred Kestenbaum (1890-1961) and his textbook.

and it was obvious that Cogan had been reading the Ger­man literature. The book was written in a very economic style so that one could pick up several important points in a single paragraph. Shirley Wray and then Simmons Lessell eventually succeeded Cogan as neuro-ophthal­mologists at the Massachusetts Eye and Ear Infirmary.

Donald J. Lyle (Fig 9) was Chair of the Ophthalmology Department at the University of Cincinnati. He worked closely with the neurologists and neurosurgeons there, pursuing his own personal interest in neuro-ophthalmol­ogy, and wrote a book of his own, Neuro-ophthalmology (early 1945, Charles C. Thomas). Donald Lyle and Frank Walsh were good friends. They were both born in 1895, both members of the American Ophthalmological Society, and, of course, Walsh was working on his own textbook of neuro-ophthalmology.

It would seem that the Nazis unwittingly made some important contributions to American neuro-ophthal­mology: Alfred Kestenbaum came to America from Ger­many in the late 1930s. He was an ophthalmologist with

Figure 11. Otto Lowenstein and Irene Loewenfeld in 1962.

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a long interest in neuro-ophthalmology, and he published the book Clinical Methods of Neuro-ophthalmic Exami­nation (1946, Grune and Stratton) (Fig 10). Thus, right after the war, four important neuro-ophthalmic books became available: in 1945, Donald Lyle's Neuro-Oph­thalmology and Cogan's Neurology of Ocular Muscles in 1946, Kestenbaum's book; and in 1947, Walsh's book.

Another immigrant who came to America in the late 1930s was the neuropsychiatrist Otto Lowenstein (1890-1965) (Fig 11). He was interested in the workings of the pupil of the eye and made many important contributions over the next decades. This was followed up by his student Irene Loewenfeld who, in 1993, completed a massive book on the subject, starting with Lowenstein's contributions. Another was Alfred Bielschowsky (1871-1940), a well­established German Professor of Ophthalmology, who in 1935 accepted an invitation from Adelbert Ames to join the Dartmouth Eye Institute. He practiced there for 5 years and lectured widely on eye movements. He died suddenly on a trip to Manhattan and was buried in Han­over, NH.

In 1959, Paul Levatin (Fig 12) emphasized the value of pupillary signs in optic nerve disease, a topic that had been important to Kestenbaum in 1946 and to Marcus Gunn in 1907 (BMJ 1:1353). This theme was picked up by Thompson in 1966 (AJO 62:860).

Frank Burton Walsh (18 Oct 1895-27 Nov 1978) was a Canadian from Saskatchewan who had served in World War I and received a shrapnel wound to his right lung that sent him back home (Fig 13). He received his medical degree from the University of Manitoba in 1921, interned in Winnipeg, and began to practice general medicine. Af­ter 7 years, he decided he wanted to specialize and began a residency at Johns Hopkins in 1930 with Dr. Wilmer as his Chief.

The head of neurosurgery at Johns Hopkins was Cush­ing's student, Walter Dandy, the man who introduced pneumoencephalography (Fig 14). Dandy wrote a book

Thompson . Neuro-ophthalmology in the 20th Century

on orbital tumors for which Alan Woods (Wilmer's suc­cessor) prepared an introduction. This suggests that there was a continuing collaboration between ophthalmology and neurosurgery at Hopkins. Walsh was particularly in­fluenced by Frank Ford (Fig 15), the pediatric neurologist who was working on the book, Diseases of the Nervous System in Infancy, Childhood and Adolescence (1937,

Figure 12. Stan Thompson visiting Paul Levatin in 1989.

Charles C. Thomas, Springfield). Walsh's 1947 book, Clinical Neuro-ophthalmology, was so impressive and so popular that he soon started working on the second edi­tion, which came out in 1957. The second edition of Walsh's Clinical Neuro-ophthalmology was bigger than the first edition, and it had a redder cover and three col­umns instead of two; it was altogether a very impressive

Figure 13. William F. Hoyt and Frank B. Walsh.

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Figure 14. Walter Dandy.

compendium of neuro-ophthalmic knowledge. It influ­enced me early in medical school to take an interest in neuro-ophthalmology, and it obviously influenced Wil­liam Hoyt, who was finishing his ophthalmic residency at the time in San Francisco.

Another book that had an influence on neuro-oph­thalmology was Polyak's The Vertebrate Visual System (1958, University of Chicago Press). Stephen Polyak (1889-1955) was an anatomist with an interest in the ret­ina. His book, completed posthumously by Kluver, in­cluded an historical review of in vestigations of the struc­ture of the eye and the visual pathway and the visual centers of the brain. It was, of course, this neuro-anatomic work that made neuro-ophthalmic diagnosis possible.

William Fletcher Hoyt was born in 1925, so he was approximately 32 when Walsh's second edition, Big Red, came out. Walsh then gave the Proctor Lecture in San Francisco, and Hoyt, who had an interest in neuro-oph­thalmology and had been helping Harrington with the visual field defect illustrations for his book, was captivated by Walsh and by his compendious book. He had promised Cordes that he would go and spend 6 months in Vienna after finishing his residency. He did this, and on his way back to the West Coast, stopped for 6 months in Baltimore to spend time with Walsh. Walsh was very much im­pressed with Hoyt and in 1962, they signed a contract with Williams and Wilkins to do a third edition of Walsh's book (Fig 13). Walsh and Hoyt finally appeared in 1969. Walsh wrote another important book in col­laboration with his friend Richard Lindenberg, who was the neuropathologist at the Baltimore City morgue, and his fellow Joel Sacks. It was called The Neuropathology of Vision, an Atlas.

Hoyt also wrote another book that was exceedingly popular called The Ocular Fundus in Neurologic Disease. In this case, his collaborator was the photographer Diane Beeston.

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The fourth edition of Walsh and Hoyt came out in the 1980s and was authored by Neil Miller of The Wilmer Institute. The dramatic increase in the size of this book through its four editions is an indicator of the geometric expansion of neuro-ophthalmic knowledge (Fig 16). "Pappy" Walsh died in 1978 at the age of 83.

The Training of Neuro .. ophthalmologists

Hoyt probably trained more neuro-ophthalmologists over the years than anyone else (Fig 17). He often had two or three fellows at a time. Sometimes, they stayed only a few months and sometimes 2 or 3 years. Richard Sogg was Hoyt's first fellow (1961-1962). Bob Hepler from Los Angeles spent a year with Cogan and then spent a year with Hoyt before returning to Los Angeles. Stan Thomp­son and Bob Hepler were fellows together in 1966-1967. Within the next 8 or 9 years, there followed a stream of people who later made their mark in neuro-ophthalmol­ogy. Among them were Robert Daroff; Michael Sanders of London; Jim Keane; Marty Lubow; James Corbett; John Susac; Todd Troost of Winston-Salem; Joel Glaser of Miami; Enrique Piovanetti of Puerto Rico; Ray Buncic of Toronto; Guntram Kommerell ofFreiburg; Lars Frisen of G6teborg; Moshe Feinsod, a Haifa neurosurgeon; Mickey Rosenberg of Chicago; Jim Sharpe, who returned to Toronto and took a particular interest in eye movement studies; Jack Selhorst, who became head of the Neurology Department at St. Louis University; Neil Miller, who suc­ceeded Walsh as the neuro-ophthalmologist at Wilmer and became the author of the fourth edition of Walsh and Hoyt's textbook; Tom Shults of Oregon; Myles Berhens of Manhattan, who trained many of New York's neuro­ophthalmologists; Pat Sweeney of Cleveland; David Tay­lor, who specialized in pediatric neuro-ophthalmology at Great Ormond Street in London; Bruce Wilson of Denver; Ivor Levy of London; Kay-Uwe Hamann of Hamburg;

Figure 15. Frank Ford.

Thompson . Neuro-ophthalmology in the 20th Century

Figure 16. The first four editions of Walsh's textbook.

and Eeva Nikoskelinen of Finland (Fig 18). This was just the first decade. In the next 2 decades, he trained a lot more fellows.

Ed Norton was best known as an educator, adminis­trator, and retina surgeon, but he trained in neuro-oph­thalmology, spending time with Cogan and then with Walsh and with Rucker. He founded the Bascom Palmer Eye Institute in Miami and built a strong neuro-oph­thalmology unit there with J. Lawton Smith as its cen­terpiece.

Lawton Smith was a resident at Wilmer with Mau­me nee and with Walsh (1955-1958) and then spent a year with Cogan in Boston. He returned to Wilmer as Chief Resident (1959-1960) and then went to join the Eye Division at Duke University. Lawton Smith was filled with energy and good spirits and was an entertaining teacher and a very effective popularizer of neuro-oph­thalmology. His message seemed to be, "This stuff may not pay very well because it is mainly descriptive, diag­nostic and non-surgical, but you learn something new every day and it sure is a lot of fun." In 1962, Norton recruited Smith from Duke University to be the neuro­ophthalmologist in the new Bascom Palmer Eye Institute

in Miami, and then Norton and Smith persuaded Peritz Scheinberg, the Chair of Neurology at Miami, to appoint Noble David to his department with support from the Veterans Administration Hospital and a little help from the Eye Department.

"Nobby" David was a neurologist with an interest in neuro-ophthalmology and a good friend of Smith's. They had spent time together with Cogan in Boston and had worked together at Duke. Norton had not lost his affection for neuro-ophthalmology, and now he had a nucleus that he knew would attract others (Figs 19-21).

Robert Daroff was a neurology resident at Yale in 1963 when he developed an interest in neuro-ophthalmology. He wrote to Walsh, inquiring about special training, but at that time, Walsh was of the opinion that neuro-oph­thalmology was a subspecialty of ophthalmology and that he should not be training neurologists. He later changed his mind. Daroff spent 3 months with Lawton Smith and apparently convinced Smith that a neurologist was worth training. Darofflater spent a year with Hoyt (1967-1968) and there nurtured his special interest in eye movement abnormalities. Nobby David helped to persuade Schein­berg to appoint Daroff to the Miami Neurology Depart­ment and helped to provide funding for an eye movement laboratory. Daroff and his biomedical engineering col­league, Lou Dell'Osso, made many important contribu­tions to the understanding of eye movements.

Todd Troost was advised by Hoyt to take a fellowship with Daroff and afterward stayed on the Miami faculty for some years before becoming Chair of Neurology at Winston-Salem, NC.

Joel Glaser was an ophthalmology resident in Miami and a student of Lawton Smith's. He spent a year with Hoyt and came back to write a popular one-volume neuro­ophthalmology textbook and to become a pillar of the neuro-ophthalmology faculty at Miami.

All this neuro-ophthalmic excitement in Miami pro­duced the largest stable of paid neuro-ophthalmologists (Norton, Smith, David, Daroff, Glaser, Troost, and

Figure 17. W . F. Hoyt in 1967 and in 1995.

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Figure 18. Some of Hoyt's fellows from 1966 to 1976. Top, Robert S. Hepler, H. Stanley Thompson, Robert B. Daroff. Bottom, Michael D. Sanders, Guntram Kommerell, Lars Frisen. (Fig 18 continues.)

Dell'Osso) under one university administration ever (Fig 22).

The neuro-ophthalmology group at the Wills Eye Hos­pital in Philadelphia started with Nathan Schlezinger, a neurologist and psychiatrist with an interest in neuro­ophthalmology who was on the volunteer faculty at Jef­ferson Medical College and at Wills Eye Hospital. Alpers

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used to send his neurology residents over to Wills to learn some neuro-ophthalmology from Schlezinger. Norman Schatz was the first neurologist to take a fellowship in neuro-ophthalmology, when he returned in 1967 to Phil­adelphia after his year with Lawton Smith, he joined Schlezinger's practice and taught the eye residents at Wills. When Schlezinger retired in 1973, a cluster of vigorous

Thompson . Neuro-ophthalmology in the 20th Century

Figure 18. (continued ) Top, Joel S. Glaser, James Sharpe, John B. Selhorst. Bottom, Neil Miller, Myles M. Behrens, David Taylor.

neuro-ophthalmologists gathered around Schatz (Fig 23). These included James J . Corbett (1973-1977), Linda Orr (1975-1977), Peter Savino (1975-), and Robert Sergott (1979- ). When Schatz retired, he went to Miami and did volunteer neuro-ophthalmology teaching with his friend Joel Glaser at the Bascom Palmer Eye Institute.

Corbett later joined Van Allen's Neurology Depart­ment in Iowa City, where he worked with Thompson from

1977 to 1991 before becoming the Chairman of Neurology at the University of Mississippi in Jackson (Fig 24).

Morris B. Bender was a New York neurologist who went to medical school at the University of Pennsyl­vania, where he was influenced by W.G. Spiller. Bender took an active interest in neuro-ophthalmology, partic­ularly in eye movement problems. He did a fellowship in neurophysiology at Yale with John F. Fulton and

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Figure 19. Edward W. D. Norton (1922-1994). Figure 21. Noble David.

was able to show in primates the features of aberrant regeneration of the oculomotor nerve that could be seen clinically in humans (Fig 25). In the 1940s, with his student Edwin Weinstein, he followed up on Spiller's suggestion that an internuclear ophthalmoplegia was caused by a lesion in the medial longitudinal fasciculus and worked out the details of the anatomy. In the 1950s, he worked with Teuber and Battersby on visual field loss with various cerebral lesions and with Stefan Shan­zer on optokinetic nystagmus, and in the 1960s with Bernard Cohen on vestibular-ocular connections. Bender made major contributions to our understanding of eye movement abnormalities. John Leigh of Cleve­land and David Zee of Baltimore wrote an excellent book on eye movement abnormalities that has become a standard reference work for the clinician.

Figure 20. }. Lawton Smith.

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Neuro-ophthalmology started in S1. Louis, when Andy Gay returned after a year with David Cogan. Gay trained John Keltner, Nancy M. Newman, and Ron Burde. When Gay moved to Maine in 1970, Burde became the neuro­ophthalmologist at Washington University in St. Louis and trained a series of fellows there before becoming the Chairman of Ophthalmology at Einstein in New York (Fig 26). Keltner was neuro~ophthalmologist at Yale be­fore becoming Chair of Ophthalmology at the University of California in Sacramento. Newman became neuro­ophthalmologist at Pacific Medical Center in San Fran­cisco.

Courses of Instruction

In the early 1970s, a course in neuro-ophthalmology was offered at the American Academy of Ophthalmology at the Palmer House in Chicago involving Hedges, Walsh,

Figure 22. Miami neuro-ophthalmologists in 1984 (David, Schatz, Nor­ton, Smith, Glazer).

Thompson . Neuro-ophthalmology in the 20th Century

Figure 23. Norman Schatz.

Cogan, and John Henderson of Michigan . A few years later, a similar American Academy of Ophthalmology course was started by Burde, Glaser, Schatz, and Savino. Neuro-ophthalmology was a popular component of the Lancaster Course in Ophthalmology, held every Summer at Colby College in Maine (Fig 27).

National Meetings

David Knox at Wilmer, at the instigation of Frank Walsh and Richard Lindenberg, started a neuro-ophthalmology­neuropathology meeting, which met every year for several years at Wilmer and which later was called the Walsh Society and still tends to have a format consisting of in-

Figure 24. James J. Corbett (1982).

Figure 25. Morris Boris Bender (1905-1983).

teresting and difficult cases, illuminated by a guest neuro­radiologist and a guest neuropathologist.

The International Neuro-ophthalmology Society was founded in 1976 by Thomas Hedges, Jr., of Philadelphia, who in 1948 had been Walsh's first fellow, and his friend Alfred Huber of Zurich, Switzerland, who had written a book, Eye Symptoms in Brain Tumors based on his as­sociation with Professor Krayenbuhl's neurosurgery ser­vice (1961). The international meeting started small at LaNapoule in the south of France and has been meeting on even-numbered years since then and growing steadily (Fig 28).

A small group of researchers and clinicians interested in the workings of the pupil of the eye have been meeting

Figure 26. Ronald M. Burde.

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Figure 27. The neuro-ophthalmology teachers at the Lancaster Course, Colby College, MA, 1977 (Norm Schatz, David Cogan, Joel Glaser, Andy Gay, John Keltner).

every other year since 1961. The meeting, called The Pupil Colloquium, was founded by Lowenstein, Loewenfeld, and Larry Stark.

Organized Neuro .. ophthalmology

In 1975, the Albuquerque neuro-ophthalmologist at the University of New Mexico, Tom Carlow, with the help of Robert Daroff, Joel Glaser, and William Hoyt, orga­nized a neuro-ophthalmology meeting in Santa Fe, New Mexico. Norm Schatz joined the group a year later (Fig 29). This was such a success that the Rocky Mountain Neuro-ophthalmology Society was formed, meeting an­nually at a ski resort. The meeting soon became a general participation meeting for neuro-ophthalmologists, and the instructional components became seminars addressed to an audience of eager neuro-ophthalmologists. In 1986, the name of the group was changed to the North American Neuro-Ophthalmology Society, and 5 years later the North American Neuro-Ophthalmology Society was merged with the Walsh Society to give North American Neuro­ophthalmology a single voice.

In 1995, the Journal a/Clinical Neuro-aphthalmolagy, which had been edited by J. Lawton Smith since it was founded in March 1981, changed its name to Journal 0/ Neuro-ophthalmologyand, under the editorship of Ron Burde, became the official publication of the North American Neuro-Ophthalmology Society. In the series published by the Academy of Ophthalmology outlining the Course on Basic and Clinical Sciences, Section V cov­ers Neuro-ophthalmology. In the American Board of Ophthalmology's oral examination, one of the six subtests covers neuro-ophthalmology. Thus, neuro-ophthalmology became an acknowledged subspecialty of both Neurology and Ophthalmology, and exposure to neuro-ophthal­mology became a required component of both training programs, and doctors in both specialties became accus­tomed to sending patients with neuro-ophthalmic prob­lems to a subspecialist who concentrated on the neurology of the visual and ocular motor systems.

In a single generation, neuro-ophthalmology in America changed from a special area of medical interest

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Figure 28. Hedges, Huber, and Knox (1980).

into a medical subspecialty. Such a change requires the conjunction of several factors, some of them institu­tional. For example, a body of neuro-ophthalmic knowledge needs to be identified; some professors are needed, who practice and teach and add new knowledge to the subspecialty; training programs in the subspe­cialty need to be established; and some well-respected in-depth textbooks in the area are needed; a certai~ minimum number of doctors, both academics and practitioners, are needed who are willing to identify themselves as this kind of sub specialist, and they should be gathered into a national society that speaks for the subspecialty; and at least one journal devoted to the subspecialty should be thriving.

Neuro-ophthalmology has done all these things and has become a legitimate medical subspecialty, but why did it sputter noisily to life in the 1960s and why did it then grow exponentially in the next 2 decades? Walsh and Cogan were the kickoff professors and Boston, Bal­timore, and Miami were the starting institutions. Walsh's second edition caught the imagination and helped to bring Hoyt, Smith, and Norton to Baltimore in 1958. That group must have warmed up Walsh's Sat­urday Morning Conferences and brought neuro­ophthalmic discussion, as Lawton Smith would say, "to fever pitch." If Norton's much-admired Bascom Palmer Eye Institute could keep several neuro-ophthal­mologists busy, then every other training program wanted one too. Hoyt's thoroughness and encyclopedic

Figure 29. The founders of the North American Neuro-ophthalmology Society, photographed in 1993 (Carlow, Glaser, Hoyt, Daroff, Schatz).

Thompson . Neuro-ophthalmology in the 20th Century

knowledge made him a natural to bring Walsh's book up to date.

The growth of neuro-ophthalmology was, however, not just because of the arrival on the scene of some vigorous and colorful personalities. It was made possible by the patronage of ophthalmology departments who were helped by largesse of the National Institute of

Health and by the extra money made available from rising surgical fees. Even if these hot bed conditions do not last forever, the value of the specialist in neuro-ophthalmology has been shown, and there al­ways will be a need for clinicians with the skill, experi­ence, and willingness to solve neuro-ophthalmology problems.

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