Brain, Vol. 123, No. 1, 3-8,
January 2000
© 2000 Oxford University Press
Brain in the twentieth century
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When the twentieth century began, Brain had already achieved its majority. It was an established part of the neurological world as a reviewing and abstracting journal, as the official organ of the Neurological Society of London (the meetings of which were reported in detail) and above all as the place where neurologists from around the world placed their important work. What kind of work did they report? In this short review I shall survey the changing concerns of neurology as they are reflected in the papers published in Brain. With a few exceptions dictated by fairness to surviving co-authors, I have identified by name only those who are deceased.
Neurology at the end of last century was conceived as a subject which subsumed all matters to do with the nervous system, both normal and pathological, in animals and in man. Clinical neurology was firmly situated within general internal medicine. Psychiatry was assumed to be within its purview. It was taken for granted that the neurologist would be a person of broad intellectual interests. Thus the reviews covered not only what we would now consider strictly neurological matters, but philosophical and psychological ones as well. Something of the breadth and flavour of the Journal and its international standing can be gauged from a consideration of a selection from the contents of those years.
From Britain, Bucknill (one of the founders) wrote a critique of T. H. Huxley on Hume (Bucknill, 1879a
) and on Balfour's `A defence of philosophical doubt, being an essay on the foundations of belief' (Bucknill, 1879b); in 1880 he reviewed Bastian's `The Brain as an Organ of Mind' (Bucknill, 1880). Crichton-Browne (another founder) wrote on mania (Crichton-Browne, 1880); Ferrier (also a founder) wrote on cerebral localization (Ferrier, 1889) and much else besides; Hughlings Jackson (the fourth of the founders) too was a prolific contributor in these years. He wrote, for example, on cerebral localization, often in the course of papers on epilepsy (e.g. Jackson, 1881) speech disorders (Jackson, 1878) and on a wide range of clinical matters (e.g. Jackson, 1879). Gowers, curiously, contributed only five original papers, none after 1880, though he did make one more appearance nearly 30 years later with his Hughlings Jackson lecture on `Special sense discharges from organic disease' (Gowers, 1909). Henry Head's massive contribution on pain in visceral disease appeared in the 1890s (Head, 1893, 1894, 1896); Horsley, like many of his contempories, wrote on cerebral localization (Horsley, 1886); Rivers, who has come to prominence again recently in Pat Barker's First World War trilogy (Barker, 1992, 1994, 1996), described a case of treadler's cramp (Rivers, 1891); and Sherrington wrote both on the spinal cord (Sherrington, 1886) and the size of the spinal canal (Reid and Sherrington, 1890) amongst other subjects.
From the Netherlands, Einthoven wrote on visual perception (Einthoven, 1893). Henschen from Sweden discussed the visual pathways (Henschen, 1893) and from Germany, Erb wrote on atrophic paralysis in the child (Erb, 1883) and Westphal on syringomyelia (Westphal, 1883). The French contributions included those of Charcot and Richer on hysteria (Charcot and Richer, 1885); and Marie on acromegaly (Marie, 1889).
From the United States, Sanger Brown wrote on ataxia (Brown, 1892); Mills wrote on cerebral localization (Mills, 1880); Weir Mitchell wrote on peripheral nerves (Mitchell, 1878); and Spiller wrote on pseudosclerosis (Spiller, 1898) and on the pyramidal tract (Spiller, 1899).
The first volume of the new century (volume 23) reflected the success of the previous 22 years and foreshadowed that of the century to come. Hitzig in his Hughlings Jackson lecture stressed that it was Hughlings Jackson's clinical observations which led to his own animal experiments that were so important in establishing the pattern of cerebral localization (Hitzig, 1900). Risien Russell, Batten and Collier described subacute combined degeneration of the cord (Risien Russell et al., 1900).
Perhaps the standing of Brain at that time is best illustrated by a single issue of volume 29 (1906), which contains papers by Hughlings Jackson himself (on cerebellar paralysis, rigidity and seizures; Jackson, 1906), Horsley (on the functions of the cerebellum; Horsley, 1906), Sherrington (on the proprioceptive system; Sherrington, 1906), Edinger (on the comparative anatomy of the cerebellum; Edinger, 1906), Holmes (in a paper in which he correctly conjectured that demyelination in the central nervous system could lead to conduction block; Holmes, 1906), Wilson (on mesencephalic pupillary ectopia; Kinnier Wilson, 1906), and Head (on afferent impulses in the spinal cord; Head and Thompson, 1906). This last paper, at 204 pages, is not quite the longest paper in the history of Brain.
In the quarter century to 1925 the papers reflected new concerns in neurology, and the emergence of a new generation of neurologists who shaped the field up to the second world war. Kinnier Wilson published his paper on hepato-lenticular degeneration in 1912 (Wilson, 1912) (a paper even longer than Head's, at 214 pages). The first world war led to important advances in our understanding of the cortical representation and vision (Holmes and Lister, 1916), the cerebellum (Holmes, 1917), the reflex functions of the spinal cord (Riddoch, 1917b), and the perception of movement (Riddoch, 1917a). Encephalitis lethargica appeared during this period; papers on its symptomatology appeared in 1920 (Walshe, 1920) and 1925 (Turner and Critchley, 1925). Disseminated (multiple) sclerosis attracted attention throughout this period with papers on its familial occurrence (Reynolds, 1904), its pathology (Symonds, 1924) and contributions in 1921 to the controversy concerning its aetiology (Birley and Dudgeon, 1921; Gye, 1921).
Physiologists also placed their work, which was broadly relevant to the human nervous system, in Brain. Sherrington, for example, wrote on proprioception (Sherrington, 1906, 1918b) and on cortical stimulation in an epileptic monkey (Sherrington, 1918a), and Adrian discussed conduction in the peripheral and central nervous systems (Adrian, 1918). Two neurosurgeons with a physiological bent, Horsley and Cushing, published on a number of topics; Cushing, for example, on visual fields (Cushing and Walker, 1915; Cushing, 1921) and tumours (Cushing, 1922) and Horsley—whose contributions ceased in 1910–1911 (he died from heatstroke in Mesopotamania in 1916)—on a variety of anatomical topics and most notably on the cerebellum (Macnalty and Horsley, 1909). This last paper was written with A. S. MacNalty who, at a meeting at the Royal Society of Medicine in 1963, related that he had worked with Horsley in the latter's house in Cavendish Square. He related how the house had formerly been occupied by Brown-Sequard. Horsley told MacNalty that the charismatic neurologist held an appalled fascination for some of the literary figures who lived nearby: he was at once an admired physician and a man who, to their dismay, carried out experiments on animals. Robert Louis Stevenson was in this group and, according to Horsley, based the character of Dr Jekyl and Mr Hyde on him. Another neurologist with literary connections was Head, whose papers on sensation (with Holmes and Rivers) appeared between 1905 and 1918 (e.g. Head and Holmes, 1911; Rivers and Head, 1908) and on aphasia between 1915 and 1923 (e.g. Head, 1923).
It is interesting to note, in passing, that a number of figures who later became famous in other fields had early papers on the nervous system published in Brain during this era. They include Miller and Banting on cerebellar stimulation (Miller and Banting, 1922), Florey on the cerebral microcirculation (Florey, 1925), Peterson and Jung on galvanometer and pneumograph studies in `normal and insane individuals' (Peterson and Jung, 1907), Thomas Lewis on `defective development of the lateral cerebellar lobes in a dog' (Lewis, 1904), and Pick on optic nerve tumours (Pick, 1901).
The period 1925–1950 was marked by further studies on human reflex function, on motor control, and the emergence of clinical neurophysiology as we now understand it. The understanding of human reflexes was, to an important extent, based on the work of Sherrington and his colleagues; his Hughlings Jackson lecture (Sherrington, 1931) reviewed some aspects of this. Walshe in particular pursued these topics, taking them from the spinal to the cerebral levels where his taste for controversy, already established in 1914 with a paper on the flexion reflex in man (Walshe, 1914) to which Babinski responded warmly in 1922 (Babinski, 1922), led to some lively exchanges with Fulton, Critchley and others. Autonomic reflex control of micturition and defaecation was explored by Barrington (Barrington, 1931) and Denny-Brown and his colleagues (e.g. Denny-Brown and Robertson, 1933). Denny-Brown's papers then, as later, were often difficult to read and legend has it that Walshe passed Denny-Brown in the corridor at the National Hospital in Queen Square shortly after one of these papers appeared and remarked that he had not yet read it and was waiting for the English translation. Kupalov, Lyman and Lukov from the Pavlov Institute wrote on conditioned reflexes (Kupalov et al., 1931) and Fulton on experimental studies of the function of the frontal lobes (e.g. Fulton et al., 1932), papers which led to controversy with both Walshe and Denny-Brown. Fulton also wrote a remarkable paper in 1928 on a case of occipital angioma which he studied with the `telephone' and concluded that a `localised increase in vascularity of the Brain occurs under appropriate sensory stimulation, or more specifically, that visual activity in man is associated with an increase in activity of the occipital lobes' (Fulton, 1928). This paper resonates with those of the last decade of this century.
Controversy was also fuelled by Walshe's series of critical reviews which appeared in the 1940s (Walshe, 1942a, b). He was Editor at the time, and as Denis Williams later recorded (Williams, 1973), the reduction in flow of papers occasioned by the second world war stimulated Walshe to produce these reviews himself.
There had been occasional papers on electrophysiology in earlier decades, but a new era began with the papers of Adrian and Matthews on the Berger rhythm (Adrian and Matthews, 1934) and on the electromyogram (by Denny-Brown and Pennybacker, 1938). A number of papers of lasting clinical value appeared during this time. They include those of Adie on tonic pupils and absent tendon reflexes (Adie, 1932), Foerster on the dermatomes of man (Foerster, 1933), and Symonds and Meadows on tumours at the foramen magnum (Symonds and Meadows, 1937). From 1919 to 1950, J. G. Greenfield, often writing with clinical colleagues, published on a wide range of pathological topics including encephalitis lethargica (Buzzard and Greenfield, 1919) olivopontocerebellar atrophy (Critchley and Greenfield, 1948), and the gangliosidoses (Greenfield and Holmes, 1925). Penfield contributed over a similar, though even longer period; he began with pathology (Penfield, 1920), but his later papers dealt with the general conclusions he drew from his pioneering work on the surgery of epilepsy (e.g. Penfield, 1954), his concept of the centrencephalic integrating system drawing, once again, harsh criticism from Walshe (Walshe, 1957).
The years 1950–1975 witnessed striking changes in the field, but first there was more descriptive neurology. Symonds described cough headache (Symonds, 1956). The paraneoplastic syndromes achieved great prominence in the 1950s and 1960s with papers from Russell Brain and his colleagues at the London Hospital (there were six in one issue in 1965) and from E. P. Richardson describing progressive multifocal leuko-encephalopathy (Åström et al., 1958).
New diseases of muscle were recognized by Shy and colleagues (Shy et al., 1963) and the metabolic basis of muscle disease began to be elucidated. There was a renewed interest in infective neurology ushered in by Greenfield's review of encephalitis (Greenfield, 1950). Most notable was the publication on the pathology of the transmissable dementias by Beck and Daniel in collaboration with Gadjusek and Gibbs (Beck et al., 1969).
Neuropsychology developed rapidly in these years with papers by Zangwill and his colleagues (e.g. Ettlinger et al., 1956), some of whom happily are still contributing to the Journal; by Geschwind (e.g. Geschwind, 1965); by Luria (e.g. Luria, 1965); and by Sperry (Gazzaniga, 1965). New understanding of peripheral neuropathy and its mechanisms began in this era through the application of biopsy and electrophysiology, particularly by the London and Mayo Clinic schools and by that of Buchthal in Copenhagen (e.g. Buchthal and Behse, 1977).
Evoked potentials became part of the standard diagnostic assessment of central demyelinating disease and indeed so numerous were the papers submitted to the Journal describing their use in a variety of conditions in the mid 1970s that an embargo was placed on them by the then Editor, Charles Phillips, unless new principles were involved.
In this period there was also a recrudescence of interest in cerebrovascular disease, with papers especially on aneurysms (both macroscopic and microscopic), vascular malformations and subarachnoid haemorrhage. Anatomical papers, both comparative and human, have been a feature of Brain since its inception. A notable series in the second half of this century is that by Marion Smith and Peter Nathan, beginning in 1955 (Nathan and Smith, 1955) and continuing to 1996 (Nathan et al., 1996), on the ascending, descending and intrinsic pathways of the spinal cord. A paper of special interest by the anatomist Alf Brodal appeared in 1973 (Brodal, 1973) in which he discussed his personal experience of a stroke and its anatomical implications.
An even more striking change in the contents of the Journal has taken place in the last quarter of the century as imaging, genetics, immunology and treatment have come increasingly to pervade neurology. The first paper on X-ray CT scanning appeared in 1975 (Ambrose et al., 1975) and represented a revolution in our ability to demonstrate cerebral tumours. The greatly enhanced diagnostic capability which resulted was extended by MRI. More recently, MRI and MR spectroscopy have been exploited to give new insights into the pathogenesis and evolution of a number of CNS diseases, particularly Alzheimer's disease, multiple sclerosis and epilepsy [which was relatively neglected in the Journal in the mid-century, apart from the contributions on temporal lobe epilepsy and its surgical treatment by Denis Williams (e.g. Williams, 1975) and Falconer (e.g. Engel et al., 1975)]. Neuroimmunology has emerged as a specialty and shed light on the cellular mechanisms of immune-mediated disorders of the central and peripheral nervous systems and muscle. At least partially effective treatments of some of these disorders have followed. There has been an enormous expansion in our understanding of movement disorders around the world, led by David Marsden and his colleagues (e.g. Marsden and Obeso, 1994), and in our ability to treat Parkinson's disease. The genetic mechanisms of many of the diseases first described earlier in the century in Brain—and elsewhere—are being unravelled, the contribution of Anita Harding to the study of the cerebellar ataxias being a notable example (e.g. Giunti et al., 1994). The importance of mutations in the mitochondrial genome in neurological and muscle disease became apparent (e.g. van Domburg et al., 1996). Papers on stroke have been strikingly frequent in the 1990s.
It is fascinating that in the last decade of this century there has been a return to the questions which occupied neurologists in the last decade of the previous century, but with the difference that new techniques are providing a greater depth of understanding of mechanism. The philosophical approach of Hughlings Jackson had been continued in the mid-twentieth century by Lord Brain (e.g. Brain, 1961). Now functional imaging and the refined methods of modern neuropsychology are revealing not only new aspects of cerebral localization, but how activity in different cortical areas is organized to mediate specific cerebral functions. Some psychiatric disorders (e.g. schizophrenia; Harrison, 1999) have returned to neurology, and there is renewed consideration of the broader cultural implications of our improved understandng of the nervous system in health and disease (e.g. Zeki and Lamb, 1994).
Looking back at the century's end over the contents of the Journal and reflecting on even the limited selection to which I have referred, one can see why in the hierarchy of the (one-year) impact factor which reflects the number of times that papers are cited, Brain is second amongst neurological periodicals, and in the 15-year impact factor (compiled by Garfield, 1998) it is first, and thirteenth amongst all science journals investigated by the Institute for Scientific Information. The success sustained to the end of this century augues well for the next.
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For a period, Hughlings Jackson hyphenated his name. We have listed all his papers under Jackson J Hughlings. The question of the hyphen is discussed by Critchley and Critchley (1998).
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