From the Archives
Symptomatology of cerebellar tumours; a study of forty cases. by T. Grainger Stewart (Registrar) and Gordon Holmes (Resident Medical Officer, National Hospital, Queen Square, London). Brain 1904; 27: 522–591. with The symptoms of acute cerebellar injuries due to gunshot injuries. by Gordon Holmes. Brain 1917; 40: 461–535. with The cerebellum of man. by Gordon Holmes. Brain 1939; 62: 1–30.Gordon Holmes, about whom Ian McDonald provides additional biographical and scientific details elsewhere in this issue, counts among the few trail-blazers who shaped neurology as a medical discipline. To begin with, Holmes structured the neurological examination, more or less in the way it is performed today, as carried out almost anywhere in the world (Holmes G. Introduction to clinical neurology. Edinburgh: E & S Livingstone; 1946). Among his many specific contributions to neurology, those on the cerebellum and the visual cortex stand out. Most of this study resulted from his work as a physician in France during the Great War, first with the Red Cross and subsequently with the British Army. Two factors prompted the many clinical observations he made in these war years. The first was Holmes' energy and sangfroid in examining countless numbers of men with head wounds, in order to gain more insight into the relationship between structure and function of the brain. He made meticulous notes of these observations and also produced tracings of movements by means of revolving drums. One can only marvel at Holmes' assiduity, given the difficult and often ghastly circumstances in the medical facilities behind the front lines where an entire generation of European youths was massacred. The second factor was the structure of the British steel helmet, which left the back of the head unprotected against shell fragments and bullets (see Fig. 1) leading to many penetrating wounds in that area, and resulting in disorders of cerebellar and visual function.
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Writing, as it were, from the battlefield in 1917 Holmes acknowledges that ‘the functional deficits which are produced by injury or disease of the cerebellum have been described by many physiologists and clinicians’. Among these previous authors are clinicians (Babinski, André-Thomas, Marie) and experimental physiologists (Luciani, Rothmann). The physiologists have the obvious disadvantage of needing to rely on observations of spontaneous behaviour, whereas the clinicians could ask their patients to perform a variety of tests. On the other hand clinicians are always handicapped since they have only limited opportunities for clinico-anatomical observations, and clinical features are often bilateral (such as in multiple sclerosis) or, in the case of tumours, cerebellar dysfunction is often accompanied by the manifestations of brainstem compression, increased pressure of the cerebrospinal fluid (with or without hydrocephalus) or meningeal irritation. These limitations also apply to the study Gordon Holmes published 13 years earlier, when he was just 28 years of age, with Thomas Grainger Stewart as first author. Only the motor deficits described in 1904 can, in retrospect, be attributed to dysfunction of intrinsic cerebellar function. The 1917 article is much more detailed in observations, and mature in interpretation, and should be regarded as the essence of Holmes' ideas on cerebellar function. The 1939 paper is a written version of the 10th Hughlings Jackson lecture, delivered before the Section of Neurology of the Royal Society of Medicine, in December 1938. He summarizes and expands the earlier observations, but also addresses issues raised by experimental physiologists in the intervening years—discussions that have now lost much of their relevance and will largely be passed over here. In the later paper, Holmes also slightly modifies some of his earlier interpretations of the clinical phenomena of cerebellar disease.
Holmes starts his ‘war paper’ (1917) by explaining that it is based on 21 patients with cerebellar injuries and pronounced symptoms who remained under observation sufficiently long to permit repeated examination. The style of the paper is narrative rather than consistently quantitative, but often he informs the reader about the number of patients or observations on which a particular assertion is based, sometimes using a separate table. The first feature Holmes discusses is the abnormality of muscle tone in cerebellar lesions. He exemplifies this by means of several tests and finds by ‘palpation, passive movement, shaking and tapping of the affected limbs, that their muscles are soft and flabby’. The phenomenon is more easily demonstrated in the arm than the leg and can persist for up to 90 days after infliction of the wound. However, while acknowledging—especially in 1939—that ‘tone’ can be defined in a variety of ways, Holmes includes in his definition of hypotonia not only the flabbiness of muscles in a relaxed state, but also the capacity of a limb to maintain a fixed position, ‘postural tone’ (see Fig. 2). Among the examples he gives are the increased displacement after tapping an outstretched arm on the side of a cerebellar lesion, and the ‘rebound phenomenon’ discussed below.
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The main abnormality after cerebellar injuries, of course, consists in disturbances of voluntary movement. Holmes distinguishes several aspects:
- Slowness in muscular contractions and relaxations. Using a dynamometric apparatus he tabulates the maximum force in several limb muscles of two patients and finds it consistently less in the affected than the unaffected side, whereas there is no disturbance of ‘static strength’, or the resistance offered in voluntary resisting displacements. That the delay is apparent not only in initiating movements but also in relaxation after a muscle has been activated is elegantly shown in a recording of a patient with a lesion of the right lateral lobe of the cerebellum whose hands are placed against two springs that are first grasped and then released (see Fig. 3). On stimulation by a faradic current, the muscles on either side react in the same way. Holmes concludes that this form of muscle weakness is not ‘paresis’ and prefers the term ‘asthenia’, introduced by Luciani.
- Ataxia. This most commonly recognized sign of cerebellar disease is not influenced by vision, other than with loss of position sense such as that occurring in tabes dorsalis. It is more striking in the arm than the leg: ‘during the movement the finger deviated from the direct course by which it could most easily reach its aim’. Holmes distinguishes several factors contributing to cerebellar ataxia: (a) decomposition of movement (movements involving different joints are broken up into separate elements; in the 1939 paper he illustrates this by means of a camera and a light attached to the moving finger—see Fig. 4); (b) asynergia (lack of proper synergism in the contraction of agonists, antagonists and fixating muscles, such as overextension of the wrist in an attempted grip); (c) dysmetria (failure to adapt the movement to its aim, in range and in force; after the first few weeks dysmetria generally takes the form of hypermetria); (d) tremor (not just the intention tremor associated with dysmetria but also after the target has been reached); and (e) deviations from the line of movement (partly but not wholly attributable to dysmetria, ‘as the hand which the patient wishes to bring to his nose often comes to his cheek or eye even when it is moved from directly in front of his face’).
- The rebound phenomenon. Holmes describes this sign, already reported with Grainger Stewart in the 1904 paper, in the following words: ‘The patient's elbows are supported on a bed or table and he is asked to pull each hand in succession towards his mouth against resistance offered by the observer who grasps his wrists; when this resistance is suddenly released the hand of the affected side flies to his mouth or shoulder, often with considerable violence, but the movement of the normal limb is arrested almost immediately by contraction of the antagonists (triceps) and may even be jerked back or rebound’.
- Adiadochokinesis. This term, coined by Babinski, represents failure to execute alternate movements such as pronation and supination as quickly and correctly as a normal person. Also other muscles may be involved than under normal conditions. Holmes notes this as one of the most persisting signs of cerebellar injury.
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All these aspects of defective movement are most apparent when the patient attempts to use simple and familiar tools, such as a pair of scissors, or a pen in writing (see Fig. 5).
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Holmes goes on to list a range of other phenomena of cerebellar disease, apart from abnormalities of tone and movement: static tremor (of the head or body, if the patient is standing); vertigo (usually a sense of rotation around the longitudinal axis, rarely persisting for more than 1 or 2 days); spontaneous deviation of the extended, unsupported arm with eyes closed (usually outward; a similar deviation occurs when a pointing test is performed with eyes closed); a tendency to veer or even fall towards the affected side; nystagmus, especially on looking towards the affected side, with the fast phase in that direction; abnormal speech (alternately slow, staccato or explosive); tendon jerks that have a normal contraction phase (as testified by recordings of the knee jerk on a revolving drum) but after which relaxation is more rapid, followed by some inert swinging, the pendular character described by André-Thomas.
Holmes concludes that the exact site of the lesion within the cerebellum has no great influence on the nature of the clinical phenomena apart from its laterality. In lesions of the vermis there are greater disturbances of phonation and articulation: tremor is more pronounced and there is greater difficulty in movements of the head and trunk on sitting up; but there is no great difference with symptoms produced by injury of both lateral lobes. He finds that with superficial lesions the symptoms disappear more rapidly than with deeper lesions that also involve the cerebellar nuclei. Of a somatotopical organization within a cerebellar lobe he has not found proof, but Holmes prefers to remain neutral on this issue for want of sufficiently detailed histological observations.
Both articles—that from 1917 with the elaborate observations as well as the 1939 Hughlings Jackson lecture having the advantage of hindsight in reviewing his subject—culminate in a perceptive discussion of the neurophysiological explanation, or, to use Holmes' own term, the ‘nature’ of the symptoms produced by cerebellar lesions. First of all he accounts for the different aspects of ‘atonia’ by referring to the physiological investigations of Sherrington and Langelaan, who have shown that ‘tone is a more complex condition than has been generally realized by clinicians’. He attributes loss of ‘postural tone’ to the Sherringtonian concept of the stretch reflex, or failure of the immediate reflex contraction of antagonists when they are suddenly stretched. In his view this would explain features such as the rebound phenomenon, absence of contraction of the hamstring muscles following elicitation of the knee-jerk, and the greater swing if the outstretched arm on the affected side is tapped. Present-day neurophysiologists are less inclined to attribute a role to segmental reflexes in the maintenance of posture; instead they favour a delayed reaction time as the main factor, i.e. the first abnormality in voluntary movement listed by Holmes. Perhaps this explanation applies even to hypotonia of relaxed limbs (see van der Meché FGA, van Gijn J. Hypotonia: an erroneous clinical concept? Brain 1986; 109: 1169–1178). It should be added, however, that in the 1939 review article Holmes reserves his judgement about the interdependence of the symptoms of cerebellar disease; only the disturbances in the rate and regularity of voluntary movement can be regarded as entirely independent.
In trying to explain these abnormalities Holmes starts off firmly by postulating: ‘A disturbance in the co-ordination of the muscles engaged in individual movements ... does not involve the creation of an abstract and fictitious entity, the principle of co-ordination.’ Instead, Holmes supposes that the cerebellum ‘takes no direct part in the processes, whether initiated reflexly or voluntarily, that produce motor effects, and that it does not augment these, but that it ‘sets’ or ‘tunes’ or regulates the activity of certain motor mechanisms, most probably spinal, so that the response to the volitional stimulus is immediate, effective and proportional to the intensity of the cerebral impulse’. A few pages later he adds: ‘It is an organ which has evolved on the afferent rather than on the motor side of the central nervous system ... it receives and integrates proprioceptive impulses from all parts of the body ... and it thus assures the correct co-operation of the separate motor centres that are concerned in individual acts.’ In 1939, he prefers to regard the basal ganglia and motor cortex rather than the spinal cord or the brainstem as targets for efferent impulses from the cerebellum, given reports by other scientists about combined ablation experiments in animals as well as new observations about the modulating influence of learning and attention on the manifestations of cerebellar dysfunction.
With regard to sensation, Holmes would have been puzzled by the contribution of Restuccia et al. (page 276) showing that unilateral cerebellar lesions are associated with abnormal event-related potentials in the sensory cortex. Physiologists in Holmes' times had similar ideas but he is adamant: ‘I have, however, examined every modality of sensation in many cases but have never found disturbances of any form.’ Although he finds that the ability to recognize the identity or inequality of weights lifted simultaneously by the two hands is affected, in that with equal weights the tendency is to call that on the affected hand the heavier, he attributes this to non-specific weakness: ‘by every paretic limb weights are adjudged heavier than they actually are, even though sensibility is unaffected’. Rather, Holmes concludes: ‘On this hypothesis there is superimposed on the postural and reflex mechanisms of the brain-stem a cerebello-striato-cortical apparatus concerned in the regulation of posture and of tone during voluntary movement. By virtue of the integration of the wealth of afferents it receives from all parts of the body and from the cerebral cortex, the cerebellum is controlling part of this mechanism.' If the term ‘feedback loop’ had existed at the time, Holmes surely would have used it!
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