HOLMES, GORDON MORGAN

(b. Dillon House, Castlebellingham, Ireland, 22 February 1876; d. Farnham, England, 29 December 1965),

neurology, neuroanatomy, clinical neurophysiology.

In a generation of gifted neurologists, Holmes was outstanding for his refinements of the clinical examination of the nervous system, which led to his inquisitive searching and original investigations of its functions. His work illuminated and clarified many uncertainties in the functions of the cerebellum, and the sensory and visual pathways in the brain. His rigorous, trenchant approach and inductive reasoning were widely admired and adopted by contemporary neurologists and physicians. In the fields of clinical diagnosis, the deductive reasoning he applied to neurological phenomena shaped clinical techniques and advanced understanding of neurophysiology for his many disciples and their acolytes.

Early Career . Born in Ireland to a Yorkshire Protestant family, Gordon Holmes was a shy, solitary child whose mother, Kathleen (née Morgan) died young. His father’s name was also Gordon Holmes. The son qualified in medicine at Trinity College, Dublin, in 1899. As a junior at Richmond Asylum in Dublin he was awarded the Dublin University Travelling Prize in Medicine and the Stewart Scholarship in Nervous and Mental Diseases in 1899. These financed a visit to Frankfurt, Germany, where for two years he studied comparative anatomy with Karl Weigert and Ludwig Edinger. After an arduous start with Edinger, a hard taskmaster, Holmes diligently acquired a remarkably detailed knowledge and experience of neuroanatomy and neurophysiology, which were to be the foundation of much of his subsequent work. When he returned to England in 1902, on Edinger’s recommendation he became Resident Medical Officer to Hughlings Jackson at the National Hospital for Paralysis and Epilepsy, Queen Square, London, which became the center of his life and work.

The National Hospital for Paralysis and Epilepsy in London was founded in 1859. Its reputation was based on the work of an unusually celebrated group of physicians, notably Hughlings Jackson and Charles Édouard Brown-Séquard. Its physicians in the early nineteenth century included Sir William Gowers, Sir David Ferrier, Sir Victor Horsley, and William Aldren Turner. Many have come to regard this period as a golden era in neurology.

Holmes obtained the MD in 1903, membership of the Royal College of Physicians, London (MRCP) in 1908, and was elected a Fellow six years later. He quickly mastered the clinical examination and developed it “to a state of well-nigh scientific perfection” (Walshe, 1966). His exhaustive yet rapid examination routine was unprecedented. He became physician to the Royal London Ophthalmic (Moorfields) Hospital and to Charing Cross Hospital. Few now appreciate that physicians of his generation worked as honoraries at their hospitals, receiving no payment for clinical work; teaching and research were likewise vocational and unpaid; their sustenance was supported solely by private practice.

With Sir Henry Head he wrote a classic paper, published in the journal Brain in 1911, “Sensory Disturbances from Cerebral Lesions.” In it they first described systematically the functions of a deeply placed gray matter nucleus—the thalamus—and its relationship to the cortex. Holmes later emphasized the importance not of showing whether a sensation was impaired or spared by a cortical lesion, but rather inquiring what qualities or aspects of sensory perception relate to the sensory cortex. It was necessary, therefore, for him to refine the sensory examination at the bedside and clinic in an unprecedented fashion, which soon was widely accepted as standard practice. So energetic and industrious was Holmes that by the outbreak of war in 1914 he had published fifty-five papers, seventeen of them in the prestigious journal Brain.

Myopia thwarted his volunteering for war service. Frustrated, Holmes joined the staff of a Red Cross hospital just behind the front line in France. His impressive work persuaded the War Office to renegotiate his disqualification. As lieutenant colonel, Holmes became consulting neurologist to the British Expeditionary Force in France. Patients with war injuries of the spinal cord and brain allowed him—in terrible conditions of dirt, cold, and exhaustion—to study the cerebellum and the visual cortex, which were exposed in soldiers whose helmets were incomplete at the back. He had to treat up to three hundred wounded men daily. Holmes performed all the neurological postmortems himself. This work culminated in eighteen published wartime papers, many written at the front in arduous conditions. Spinal injury was the basis of his Goulstonian Lecture to the Royal College of Physicians in 1915. He was twice mentioned in dispatches and was awarded the Order of St. Michael and St. George in 1917 and Commander of the British Empire in 1919.

Clinical Techniques . After World War I, Holmes continued in neurological practice and research. He was thorough and relentlessly precise in his methods of clinical diagnosis, though notoriously impatient with less gifted colleagues. “In teaching,” F. M. R. Walshe said in his Biographical Memoirs of the Royal Society, “he had the great gift of making clear to his students the thread of his thoughts and the grounds on which he reached his conclusions. He never posed as an oracle or a maker of slick diagnoses. … To be trained by him was a severe but most salutary discipline” (1966, pp. 311–319).

Gordon Holmes developed the foundations of modern neurological examination. He divided the examination into cortical functions, cranial nerves, motor and coordination, sensibility, and reflexes. “He could coax physical signs out of a patient like a Paganini on the violin,” observed a colleague, who continued: “every neurologist alive today … is unconsciously utilizing the routine clinical examination propagated, perfected, and perpetuated by Gordon Holmes. It was a sheer delight to watch him evoking one physical sign after another in a patient with say, tabes” (Critchley, 1979, p. 230). (Tabes is caused by syphilis of the nervous system, noted for widespread abnormalities of sensation, pupils, and reflexes.)

Holmes wrote many critical clinical papers, and with W. J. Adie he discovered the myotonic or Holmes-Adie pupil (small asymmetrical pupils that contract very slowly to convergence but not to light stimuli; they can mimic syphilitic pupils). His Introduction to Clinical Neurology(1946) was a classic, succinct textbook for students. It was not intended as a description of various diseases, but rather as a discussion of the nature and the significance of the symptoms and abnormal signs that a patient with a nervous disorder may present. It assumed a basic knowledge of anatomy and physiology of the nervous system and subsumed brief accounts of the current views on disordered function. In the foreword he said: “Though tomorrow may disprove some of them, they are put forward in the belief that ‘truth comes more readily from error than from confusion.’” With rare exceptions, he deliberately provided no authorities and no references, probably because it was a short textbook for students, who in those days were not encumbered by numerous and tedious references to papers they were unlikely to consult.

The Cerebellum . Among his many contributions. Holmes challenged the accepted theory of the workings of the cerebellum, the “corrugated” lobular structure at the back of the head that controls balance and coordinated movements. With T. Grainger Stewart he described the rebound phenomenon in cerebellar disease, later known as the Stewart-Holmes sign. He also described an inherited degenerative cerebellar ataxia involving the olivary nucleus, known as Holmes’ syndrome, and expounded the range of symptoms of cerebellar tumors. He also published a painstaking account of a form of familial degeneration of the cerebellum with a detailed review in which he attempted to classify cerebellar disease. He characterized cerebellar disturbances by asthenia (weakness), ataxia (incoordination), rebound, and adiadochokinesia (inability to perform fine alternating movements). In an excellent biographical review, Caoimhghin S. Breathnach points out how similar was his style and strategy to that of Sir Charles Sherrington, the foremost neurophysiologist of the day. “Holmes,” he said, “was as much physiologist as neurologist, a duality which should occasion no surprise when his training, so like his friend Head’s in ‘basic science’ is recalled. Under Ludwig Edinger’s guidance he had been initiated into the intricacies of functional neurohistology” (Breathnach, 1975, pp. 194–200).

Holmes’s notions of the function of the cerebellum were largely original and of major physiological importance. He believed that the cerebellum ensures the regularity and maintenance of muscular contractions and the immediate and effective response of mechanisms to cerebral impulses; it also exerts a regulating and coordinating influence on the motor centers that affect voluntary movements and by this means ensures their harmony, precision, and correct range of movement.

This did not mean, Holmes emphasized, that the cerebellum puts into play the muscles necessary for the accomplishment of complicated movements. It was an organ that had evolved on the sensory, receiving (afferent) side, rather than on the motor side of the central nervous system. But it received and integrated impulses related to position sense from all parts of the body, and by virtue of these it kept the motor mechanisms in such a state of “tone” that they could react promptly and efficiently to voluntary impulses, and it thus ensured the correct cooperation of the separate motor centers that are concerned in individual acts (Holmes, 1927 and 1939).

Visual Disorders . With Henry Head, Holmes investigated both the sensory and visual pathways and the optic thalamus. The results were published in 1911 and were reprinted in Head’s Studies in Neurology(1920).

Two outstanding problems faced doctors of the day. First, the main central area of vision in the retina lies in the macula (fovea), but its exact representation in the visual cortex was not known. Secondly, there was little understanding of those strange (agnosic) defects of appreciation of size, shape, texture of objects, and the location of the body and of external objects that often result from disease or injury to the parieto-occipital lobes at the back of the brain and which hamper recovery of movement. In his first Montgomery Lecture, in ophthalmology at Trinity College, Dublin, in June 1919, “The Cortical Localisation of Vision,” he elucidated macular vision and its sparing in injuries of the occipital lobes:

the type of blindness that is produced by superficial injuries of both occipital lobes—that is, by wounds that injure the posterior parts of the striate areas. In all such cases we find peripheral vision intact and central vision abolished. They are consequently evidence that central or macular vision is represented in the most posterior parts of the visual areas, and that this region is not concerned with peripheral sight. (p. 194)

The hemianopia (loss of the same half-fields of vision, i.e., to the right or to the left) due to vascular lesions differed from that produced by penetrating gunshot wounds in that the macula is spared. He explained this by observing that at the posterior end of the striate area of the visual cortex, the middle and posterior cerebral arteries meet so that the macula gets the benefit of their overlap. The fovea also gets the larger share of cortical retinal representation. It is probable, he said, that the portion of the striate area that frequently spreads over the occipital pole and on to the outer surface of the brain may be the center of macular sight. The frequency of paracentral scotomata (blind spots near the central visual fields) is consequently accounted for by the more exposed position of this part of the visual area than of that which lies on the inner surfaces of the hemispheres. Not only is each segment of the retinae represented in a definite portion of the visual cortex, but this representation is fixed and immutable, so that if a part of the visual cortex is totally destroyed, there will be a permanent blindness of the corresponding segment of the visual fields.

The second lecture dealt with visuospatial perception. He noted that patients who were unable to recognize the spatial relation between objects and their own bodies were also unable to determine accurately the relative positions of two objects. Patients could not accurately assess size, shape, or length of objects that they saw and could not localize them in space. They also had impaired topographical memory of familiar places, but stereoscopic vision of the thickness and depth in solid objects was often preserved. Holmes said:

In all my eight cases the condition described above was associated with gunshot wounds of the head which involved the posterior and upper parts of both parietal lobes. (1919b, pp. 230–233)

In two instances of postmortem examination, the outer surfaces were injured while the missiles passed through the inner or mesial surfaces. This was an important contribution to visuospatial function, published in 1918 as “Disturbances of Vision by Cerebral Lesions,” which he located by damage of the occipital and parietal lobes of the brain. This work facilitated both clinical analysis in trauma and other pathological conditions and the understanding of the physiological mechanisms of the visual pathways.

Spinal Injuries . Based on work at the front with the surgeon Percy Sargent, at Boulogne, Holmes gave the Goulstonian lectures at the Royal College of Physicians of London in 1915. He had handwritten notes made on site from more than three hundred spinal cord injuries. He described signs of injury to the cord and sympathetic chain, hypothermia, and the unusual occurrence of shingles (herpes zoster) in the upper margin of the sensory loss.

A partial cervical spinal cord lesion that presented with paralysis of the arms but spared the legs was another curiosity that Holmes deduced was caused by “softening,” with damage to the gray matter of the cord. Based on his extensive knowledge of pathology, he provided a systematic account of the neuropathological changes after the injury. He observed in some cases that early swelling of nerve fibers distant from the primary site of damage accounted for deterioration days or weeks after injury. Cord hemorrhage and cell death might lead to spinal cord cavities (syringomyelia). Holmes recognized that spinal “concussion,” the transient state of paralysis and impaired sensation in the legs (often regarded as nervous or hysterical), was caused by tissue changes without external evidence of injury, such as in troops buried by shell explosions. The diagnosis had to be confirmed by clinical evidence of cord damage.

Honors . In addition to a heavy clinical, teaching, and research workload in the hospital, from 1922 to 1937 Holmes was editor of Brain, the most esteemed of neurological journals. His writings on neurology touched on almost every aspect of the subject and were widely regarded as authoritative. Holmes was examiner, councillor, and censor for the Royal College of Physicians. His pre-eminence was recognized by his election as a Fellow of the Royal Society in May 1933.

He received several honorary university degrees: DSc, Dublin, 1933; DSc, National University of Ireland, 1941; the DCL, Durham, 1944; and the LLD, Edinburgh, in 1952. Retirement came in 1941, knighthood, belatedly in 1951. After enduring the London blitz, he moved to a country house in Farnham, where his passions were his garden and golf, which he played with his devoted wife Rosalie. Aged eighty-nine, his quietus came during sleep on 29 December 1965.

Holmes the Man . Words such as volcanic, tornado-like, brusque, and demanding were sometimes applied to describe him by his pupils. He had boundless energy, but was prone to migraine and duodenal ulcer. Holmes had strong likes and dislikes and no great gift for wit, diplomacy, or compromise. He was an irascible martinet devoted to detailed observation and collection of data. At the front, he disagreed with Harvey Cushing, the celebrated but short-tempered American neurosurgeon, about the treatment of casualties. His notorious feud with Kinnier Wilson, a senior, brilliant clinician and teacher at Queen Square, was related by his house-physician Macdonald Critchley: “Wilson was a vain and touchy man, jealous of Holmes, and he would ostracise anyone who stayed in the other camp. Holmes for his part could not care less, and simply ignored his colleague (Critchley, 1979, pp. 228–235).

Critchley relates the story that whenever Holmes and Wilson made their respective rounds in Queen Square, each with his own retinue of doctors of all ranks, and they met in the passageways, neither of them would budge to make way for the other party. Lengthy blockages ensued. However, despite his manner, he nevertheless inspired affection. And, he warmly entertained many loyal and distinguished medical friends, among them: Godwin Greenfield, Sir Percy Sargent, Charles Beevor, Sir Henry Head, Wilder Penfield, Sir Francis Walshe, William J. Adie, and Sir Charles Symonds. Critchley said of him: “among these [physicians at Queen Square] was that Colossus, physical as well as intellectual, Gordon Holmes who shone brightest among the galaxy of stars surrounding him” (Critchley, 1979, pp. 228–235). Walshe noted Holmes’s great gift of making clear to his students the thread of his thoughts and the grounds on which he reached his conclusions. Penfield, the celebrated Canadian surgical pioneer of brain localization, in 1971 noted his softer side, remarking that Holmes was one of the finest teachers he had known; beneath the exterior of a martinet there was an Irish heart of gold.

Holmes was truly modest and could not bear to hear his achievements or formidable reputation discussed in public; on occasion he was so embarrassed that he would leave the room. He eschewed committee meetings and many social engagements whenever possible. Contemporaries thought that Holmes resembled Sir William Gowers more than Hughlings Jackson, his first teacher at Queen Square, showing the same patient, punctilious methods of collecting clinical data, then correlating them with anatomy and pathology. Critchley’s obituary notice recorded:

“many neurologists treasured the memories of their apprenticeship to one of the giants of neurology, and to a staunch, fundamentally warmhearted counsellor and guide. In his profession, as in his garden, Holmes planted seeds for the profit and wonderment of generations to come. (“Obituary Notice,” 1966, p. 111)

Many accounts of Gordon Holmes overlook his leisure activities. He was an enthusiastic if untalented golfer; he spent long summer holidays in his native Ireland, often working on his father’s farm, pursuing his avid interest in gardening. He loved to row on the Thames at Foley Bridge. Before appointment to Queen Square he arranged a meeting with Captain Robert Scott, hoping to join his Antarctic expedition; but an Achilles tendon injury forced Holmes reluctantly to withdraw; he was able only to wave farewell at the quayside in 1910. None of Scott’s ill-fated party returned. Holmes was devoted to the works of William Shakespeare, and would read passages of poetry each night on retiring.

The life and work of Holmes is the subject of many encomiums and eulogies, which contain details and appraisals of his original, invaluable writings. His wife Rosalie (née Jobson) was an Oxford graduate, an accomplished athlete, and an international hockey player. She and their three daughters provided a close family life at 9 Wimpole Street, London, where they gave unfailing support to him in his demanding work. Gordon Holmes, though at times acidulous, remote, and difficult, exemplified an inspiring, immensely gifted man of an independent spirit and selfless dedication to his science. He left a unique legacy to all those who treat and to those who suffer from diseases of the nervous system.

BIBLIOGRAPHY

WORKS BY HOLMES

With T. Grainger Stewart. “Symptomatology of Cerebellar Tumours: A Study of Forty Cases.” Brain 27 (1904): 522–591.

“A Form of Familial Degeneration of the Cerebellum.” Brain 30 (1907): 466–489.

“Review: An Attempt to Classify Cerebellar Disease with a Note on Marie’s Hereditary Cerebellar Ataxia.” Brain 30 (1907): 545–567.

With Henry Head. “Sensory Disturbances from Cerebral Lesions.” Brain 34 (1911): 102–254. Reprinted in Studies in Neurology. Vol. I, edited by Henry Head. London: Oxford University Press, 1920.

———. “A Case of Lesion of the Optic Thalamus with Autopsy.” Brain 34 (1911): 255–271. Reprinted in Studies in Neurology. Vol. I, edited by Henry Head. London: Oxford University Press, 1920.

“Disturbances of Vision by Cerebral Lesions.” Brain 40 (1918): 461–535.

“The Montgomery Lecture in Ophthalmology. I. The Cortical Localisation of Vision.” British Medical Journal 2 (1919a): 193–199.

“The Montgomery Lecture in Ophthalmology. II. Disturbances of Visual Space Perception.” British Medical Journal 2 (1919b): 230–233.

“On the Clinical Symptoms of Cerebellar Disease.” Croonian Lectures. Lancet I (1922): 1177–1182, 1231–1237; II: 59–65, 111–115.

“A Symposium on the Cerebellum.” Brain 50 (1927): 385–388.

“Partial Iridoplegia Associated with Symptoms of Other Diseases of the Nervous System.” Trans Ophthalmic Society UK 51 (1931): 209–228.

“The Cerebellum of Man.” Brain 62 (1939): 1–30.

Introduction to Clinical Neurology. Edinburgh: Livingstone, 1946.

OTHER SOURCES

Breathnach, Caoimhghin S. “Sir Gordon Holmes.” Medical History 19 (1975): 194–200. An excellent account of Holmes’s work, especially on visual defects.

Critchley, Macdonald. “Gordon Holmes, the Man and the Neurologist.” In his The Divine Banquet of the Brain, 228–235. New York: Raven Press, 1979. A beautifully written, detailed essay about the man and his professional relations.

Fishman, Ronald S. “Gordon Holmes, the Cortical Retina, and the Wounds of War.” Documenta Ophthalmologica 93 (1997): 9–28.

Lyons, J. B. “Sir Gordon Holmes: A Centenary Tribute.” Irish Medical Journal 69 (1974): 300–302. A tribute revealing Holmes’s professional prowess and his Irish connections.

Munk’s Roll: Lives of the Fellows of the Royal College of Physicians of London. Vol. 5, edited by Richard R. Trail. London: Royal College of Physicians, 1968.

“Obituary Notice: Sir Gordon Holmes.” British Medical Journal 1 (1966): 111–112. Includes contributions from Macdonald Critchley and Francis M. R. Walshe.

Parsons-Smith, B. Gerald. “Sir Gordon Holmes.” In Historical Aspects of the Neurosciences, edited by Rose F. Clifford and W. F. Bynum. New York: Raven Press, 1982. A superb essay containing many anecdotes and personal insights.

Pearce, J. M. S. “Sir Gordon Holmes (1876–1965).” Journal of Neurology, Neurosurgery and Psychiatry 75 (2004): 1502–1503.

Penfield, Wilder Graves. “Sir Gordon Morgan Holmes (1876–1965).” Obituary. Journal of Neurological Sciences 5 (1967): 185–190.

———. “Lights in the Great Darkness.” Journal of Neurosurgery 35 (1971): 377–383.

Walshe, Francis M. R. “Gordon Morgan Holmes, 1876–1965.” In Biographical Memoirs of Fellows of the Royal Society. Vol. 12. London: Royal Society, 1966. A typically erudite biography.

J. M. S. Pearce