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1 29 Section ofneurology 993 GiHiatt R W & Willison R G (1962) J. Neurol. Neurosurg. Psychiat. 25, 11 Gombault A (1880) Arch. Neurol., Paris 1, 11, 177 Jopling W H & Morgan-Hughes J A (1965) Brit. med. J. ii, 799 Kaeser H E & Lambert E H (1962) I Int. Congr. Electromyography (Electroenceph. clin. Neurophysiol. Suppl. 22), p 29 Klinghardt G W (1966) V Int. Congr. Neuropath. (in press) Lambert E H (1962) I Int. Congr. Electromyography (Electroenceph. clin. Neurophysiol. Suppl. 22), p 9 Mawdsley C & Mayer R F (1965) Brain 88, 335 Morgan-Hughes J A (1965) Riv. Pat. nerv. ment. 86, 253 Pekelharing C A & Winkler C (1893) Beriberi: Researches concerning its nature and cause, and the means of its arrest. Trans. J Cantlie. London Rexed B (1944) Acta psychiat. scand. Suppl. 33 Rushton W A H (1951) J. Physiol. 115, 101 Sala E (1962) I nt. Congr. Electromyography (Electroenceph. clin. Neurophysiol. Suppl. 22), p 50 Simpson J A (1962) In: Modern Trends in Neurology. Ser. 3. Ed. D J Williams. London; p 245 Swank R L (1940) J. exp. Med. 71, 683 Thomas J E & Lambert E H (1960) J. appl. Phys. 15, 1 Thomas P K & Lascelles R G (1965) Lancet i, 1355 Ulrich J, Esslen E, Regli F & Bischoff A (1965) Dtsch. Z. Nervenheilk. 187, 770 Vizoso A D (1950) J. Anat., Lond. 84, 342 Vizoso A D & Young J Z (1948) J. Anat., Lond. 82, 110 Webster H de F (1962) J. Neuropath. exp. Neurol. 21, 534 Professor John A Simpson (University of Glasgow) Disorders of Neuromuscular Transmission Electrodiagnostic techniques should be used to explore the physiological properties of normal and pathological states of the lower motor neurone or muscle and not to make a nosological diagnosis. Measurement of the strength-duration relationships of electrical excitability and conventional electromyography provide information about (a) degeneration of peripheral nerve axons and muscle fibres, (b) the recruitment and frequency pattern of motoneurones, and (c) the muscle fibre constitution of motor units. From these data it is possible to decide whether muscular weakness is neural or myal (Simpson 1962). Measurement of nerve conduction velocity adds another parameter. Pathological slowing of conduction is probably due in the main to abnormality of the myelin-sheath of peripheral nerve fibres (Simpson 1964). If these studies, with the electromyographic evidence of axonal branching, point to a primary lesion of the lower motor neurones, the neurologist would like to have further information about the site of the lesion - is it polioclastic, axonal or at the neuromuscular junction? Some help may be obtained from a study of the muscular response to repeated stimulation of its motor nerve (Simpson & Lenman 1959, Simpson 1960a). Stimulation and recording techniques are conventional. The stimulus must be brief and supramaximal and the muscle response is recorded with surface electrodes to integrate the electrical activity of a volume of muscle since the area of the response is assumed to be proportional to the number of responding muscle fibres for any particular rate of stimulation. If the muscle tension is recorded isometrically by a strain gauge it will be seen that the amplitude of the evoked potential does not bear the same relationship to the twitch tension at all rates of stimulation. The decreased amplitude at fast rates of stimulation is due to restimulation within the refractory period of the muscle (Farmer et al. 1960). Movement artifacts are minimized by splinting the limb during stimulation but some artifact of this type is almost inevitable in routine diagnostic studies. Normal Neuromuscular System Stimulation of a motor nerve at rates above 12/sec in the normal subject causes the evoked muscle action potential to increase progressively with the first 3-5 stimuli. This is accompanied by progressive shortening of the duration of the action potential, particularly the second phase of the diphasic deflection. It is probably due to improved synchronization of the muscle response (Harvey & Masland 1941, Simpson & Lenman 1959, Farmer et al. 1960). At sec from the start (irrespective of the rate of stimulation) there is often a temporary decrease in amplitude of about 30% which is due to an artifact of movement. The action potential then remains at a constant level for a considerable period which depends on the frequency of stimulation. These normal increments and degrements must not be mistaken for the pathological types described below. If fast stimulation is continued the muscle potential slowly decrements but does not disappear although the muscle contraction may cease from fatigue (Merton 1954). Decrement to 50% may occur in 30 seconds with supramaximal stimulation at 50 shocks per second but often takes much longer. If stimulation is interrupted and resumed there is no obvious post-tetanic potentiation. When tetanization is repeated with rests of 1-2 seconds there is no recovery of the earlier amplitude unless the stimulus frequency is reduced. This decrement is absent or long delayed at rates below 15/sec unless this is preceded by 'fatigue' induced by more rapid stimulation. Pathological Decrement of Response In partial denervation the amplitude of the evoked muscular response is always diminished in proportion to the fall out of motor units. Premature progressive decrement of the response is less common and occurs in several disorders.
2 994 Proceedings ofthe Royal Society ofmedicine Myasthenic Reaction The most striking feature of the evoked muscle potentials in myasthenia gravis is a rapid decrement in amplitude which occurs earlier than in normal subjects and may be visible in the first few responses even at rates of stimulation as low as 3/sec. This is not an invariable finding and it may not be marked until tetanization has been repeated several times within a short period or after a similar period of voluntary contraction of the muscle (Fig 1). When it appears, the time constant of the decrement in amplitude decreases progressively with successive tetani. The rate of fall is faster with more rapid stimulation. Other responses which are commonly seen in myasthenia gravis are: (1) Initial rapid decrement with continuation of nondecrementing response at submarginal level (Fig 2B). (2) Initial rapid decrement followed by recovery of amplitude for 2-3 sec then continuing decrement (Fig 2c). (3) Progressive decrement at slow rates of stimulation (3-10 c/s) but progressive increment at faster rates of stimulation (Fig 2D). (4) Progressive increment from the start of tetanization or after a decrementing response to the first 3-5 shocks (Simpson 1960b). Types (3) and (4) are usually seen in muscles without clinical evidence of myasthenia in an early stage of the disease or in remission. If stimulation is continued these muscles usually show the delayed decrement sooner than normal muscle. After tetanization the amplitude of the action potential of a single twitch response recovers within a second and may be greater than the first response to the original train of stimuli (post-tetanic facilitation), but after successive faradizations with brief rest periods (about one second) the recovery becomes progressively * V0_i"W"N----ow[..;..;LLEL_~~~~~~~~~~~~~~~~~~~... ~~~~~~~~~~~~~ [ Fig 1 Myasthenia gravis. Recording continuous apart fronm brief breaks ofdurations indicated on trace. Supranmaximnal stimulationi of right ulnar nerve at 4 and 50/sec showing delayed inyasthenic response and post-tetanic facilitationt slower and even twitch responses may be decreased (Fig 1). Desmedt (1958) has named this 'post-activation exhaustion' and considers that it is the cause of the weakness seen clinically in the myasthenic muscle. Fig 2 Myasthenia gravis. A, classical response. B, imnmediate decrement then maintained level of response. C, decrement temporarily restored by facilitation. D, decrement at 8 stimuli/sec, progressive increment at 50/sec
3 31 Section ofneurology 995 Fig 3 Dermatomyositis. Decrementing response at 50 stimuli/sec It will be seen that the post-activation response of the myasthenic neuromuscular system shows facilitation as well as exhaustion components which combine in different ways as they respond individually to different rates of stimulation. The decrementing response may be abolished by administration of anticholinesterase compounds but the greatest response obtained may remain less than in an equivalent normal muscle. Symptomatic Myasthenias In dermatomyositis, polymyositis, and systemic lupus erythematosus there are similar muscular responses to neural stimulation but they differ quantitatively from true myasthenia gravis. The most common finding is a rapid decrement of the evoked action potential but this is rarely seen with stimulation at rates less than 10/sec (Fig 3). The decrement may be delayed by injection of edrophonium or neostigmine in some cases, but in my experience the improvement has never been so spectacular as in myasthenia gravis and it is often absent. On resuming slower rates of stimulation, the xecovery is usually slower and posttetanic facilitation usually absent. On the other hand the early facilitation effect during faradization is often marked and in a few cases exceeds anything seen in myasthenia gravis. On voluntary contraction the same slow augmentation of the electromyogram may be seen, corresponding with increased tension of the dynogram (Simpson & Lenman 1959, Simpson 1960a). The nature of the acquired myopathy in the following case is obscure. Case 1 (MN 2803) Man aged 64 when seen in 1957 In 1951 he had thyrotoxicosis treated with methyl thiouracil. In 1952, following acute respiratory infection, he developed increasing weakness and wasting of all limbs, mainly proximal, and bilateral ptosis. Tendon reflexes virtually disappeared. Equivocal response to neostigmine. No improvement with ephedrine, potassium or guanidine. Subjective improvement on pyridostigmine 240 mg daily. Worsened by ACTH or cortisone. 1953: No response to faradism. Galvanic threshold raised. 1954: Normal biopsy of right deltoid muscle. 1957: EMG (right biceps): marked insertion activity; myopathic pattern; normal conduction velocity of right ulnar nerve; normal silent period. Harvey-Masland test (right abductor digiti minimi) showed no abnormal fatigability although the potential evoked by 5/sec stimulation was lower than that at 0-5/sec. On supramaximal stimulation at 50/sec the evoked potential increased rapidly to 300% of the original level. With continued stimulation this decremented to about 50% but when the stimulus frequency was suddenly reduced the potential rapidly increased again to 200%. When stimulation was stopped for 10 sec the potential returned to 80% of the original level (Fig 4). 1964: He had gradually recovered and was now normal for his age. Harvey-Masland test normal. Anticholinesterase medication discontinued. 1965: Remains well. No evidence of neoplasm of any organ. D A V I stimulus rate.j oa after 10 sec suddenly reduced rest p.s. Fig 4 Case 1 Successive groups of ten superimposed muscular responses during indirect supramaximal faradization at SO/sec arranged serially to show marked increment followed by progressive decrement. Sudden reduction to /K S/sec stimulation causes renewed 'V ~0-1 sec' increment. After a 10 second rest the response to slow stimulation is the same as original response. Time 0.5 I calibration refers to duration of p.s. action potentials
4 } - s 3 s ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~..i.si::_......::.: 996 Proceedings ofthe Royal Society ofmedicine r~~~~~~~~~~~ ::;.....:;.::.:...::::......: v-. _-~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ Carcinomatous Myasthenia Eaton & Lambert (1957) and Rooke et al. (1960) have used the term 'myasthenic syndrome' for the muscular fatigability which may be associated with carcinoma of the bronchus. They showed that the electromyographic response to a single maximal nerve stimulus is greatly reduced in amplitude. A transient further depression may occur during slow rates of stimulation but a marked incrementing response is found at higher rates of stimulation (Fig 5). Post-tetanic facilitation is a prominent feature and this is followed by a period of post-tetanic exhaustion similar to that seen in myasthenia gravis. The response to anticholinesterase drugs is inferior to myasthenia gravis and often disappears as the disease progresses. The electromyographic and pharmacological reactions do not appear to differ except in degree from polymyositis (Simpson & Lenman 1959). Neuronopathies In the majority of cases of partial denervation the muscular response to faradization is normal. In rare cases of peripheral neuropathy a decrementing response to serial stimulation may be seen (Pinelli 1957). We have reported this in diabetic neuropathy, Guillain-Barre syndrome, and in post-zoster motor neuropathy (Simpson & Lenman 1959, Simpson 1962) (Fig 6). Fig 5 Carcinomatous myasthenia. Submaximal response with decrement to 2-3 stimuli/sec. Progressive increment at 50/sec During conventional electromyographic investigation of the atrophic small muscles of a hand affected by amyotrophic lateral sclerosis, one frequently observes that some of the remaining motor units (identified by coaxial needle electrodes) show rapid decrement in amplitude during voluntary contraction (Fig 7A) (Simpson & Lenman 1959, Lambert & Mulder 1957). In some cases faradization of the ulnar nerve at the wrist with supramaximal stimuli causes rapid decrement of the action potential of a single unit. The action potential of the ulnar nerve recorded simultaneously at the elbow shows no decrement even when the muscle potential has disappeared (Fig 7B) indicating that the latter is not caused by failure to stimulate the nerve. Similar decrementing response to serial stimulation has been reported in anterior poliomyelitis (Buchthal & Honcke 1944, Hodes 1948). Pinelli (1957) reported a decrementing response to faradization of a peripheral nerve in one case of syringomyelia and one of multiple sclerosis but only with very rapid stimulation (100/sec). Recruiting or incrementing responses to faradization are not widely recognized in diseases of the lower motor neurone or muscle. Simpson & Lenman (1959) described an unusual case of bulbar and shoulder girdle palsy. Fig 6 Peripheral neuritis. Decre- 1A menting response -:-.. to fast tetanus
5 33 Section ofneurology 997 ( 5.. f.;..;... (; e~~~~ ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.. ~... S ;- _LZ.- _~~~~~~ ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ IP i- - l i.. : : : : : : l..-~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ : :..:..... Fig 7A Amyotrophic lateral sclerosis. Single unit of 1st dorsal interosseous muscle showing decrement on voluntary contraction (a) and indirect faradization (b)...f.fysuft,tfl5 JU. Fig 7B Ten superimposed ulnar nerve potentials (a) persist after muscular response (b) has disappeared with faradization at wrist A,; t% Nerv fre-%.4.fl O-S' S. 50 RF 0-2seC, favt ut Fig 8 Case 2 Recording as kw ' ftvp in Fig 4 showing increment preceding decrement on t _ faradization (50/sec). The O*5 ulnar nerve action potential p.s. (antidromic) does niot vary Case 2 (MN 2801) Woman aged 58 In 1957 she had progressive dysarthria after pharyngitis. Four months later she had slight facial weakness and loss of power in all limbs, mainly proximal. No sensory loss; tendon reflexes brisk, plantar reflexes normal. Occasional fasciculation. Not improved by edrophonium, neostigmine, ephedrine, prednisolone, or a-tocopherol. Thyroid function normal. Chest X-ray normal. 1957: EMG (right deltoid and biceps): no spontaneous activity; myopathic pattem. Normal conduction velocity (left ulnar nerve). Stimulation at 50/sec caused progressive increase of potential evoked in abductor digiti minimi to 160% then progressive decrement to 50% in the next 65 seconds but resumed its original amplitude almost immediately when the rate of stimulation was reduced to 0 5/sec (Fig 8). Muscle biopsy was normal. 1958: Progressive muscular atrophy, mainly distally. Tendon jerks became exaggerated and plantar reflexes became extensor. 1959: Died twenty-one months after onset. Postmortem confirmation of motor neurone disease. No evidence of neoplasm of any organ. Hereditary and Metabolic Myopathy In hereditary muscular dystrophy the amplitude of the evoked action potential of muscle may be lower than normal at rapid rates of stimulation but the difference is probably not significant and the time course of the later decrement is normal if faradization is continued. In chronic hypoxia the decrement may occur earlier than normal and the amplitude fluctuates irregularly. The antidromic nerve action potential simultaneously recorded does not fluctuate so the variability is unlikely to be caused by mqvement of the stimulating electrode. I have not studied this condition sufficiently to be dogmatic about these
6 998 Proceedings ofthe Royal Society ofmedicine 34 findings but if recording artifacts can be excluded the findings suggest intermittent response of muscle fibres rather than a systematic disorder of junctional transmission (Simpson 1960a). In chronic hypokalemic states there is abrupt loss of response of a proportion of the muscle fibres followed by abnormally early decrement of the remainder (Simpson & Lenman 1959). DISCUSSION Stimulation of a normal motor neurone releases more acetylcholine than is required to cause maximal endplate depolarization. This provides a 'safety-factor' so that the amount released remains adequate for full response despite gradual reduction with each of a train of stimuli unless this is continued for a long period (the duration depending on the frequency of stimulation). The amount released presumably depends on the stores of preformed acetylcholine in the nerve terminals, possibly in a bound form, and on the rate of synthesis by choline acetylase. Synthesis may be effected throughout the whole length of the nerve fibre from its cell of origin, or it may be formed in the cell body and transported distally along the axon by protoplasmic flow (Hebb & Waites 1956). Defective synthesis or release of acetylcholine might therefore be expected in lower neurone disorders whether the pathology is mainly polioclastic or distal. The comparative rarity of the myasthenic phenomenon in disease of the lower motor neurone probably indicates that the critical state of 'absent safety factor' is present during a relatively short period of neuronal degeneration. This would also account for the occasional reports of favourable response to neostigmine in disorders of the lower motor neurone. The excess of acetylcholine over that required for full muscular response produced by faradization of a normal nerve obscures the facilitation effect of a tetanus. The potentiation is believed to be a pre-junctional effect which increases the efficiency of ejection of acetylcholine by the nerve terminals (Liley 1956). It is, accordingly, of some interest that early tetanic and posttetanic facilitation have been reported in amyotrophic lateral sclerosis (Simpson & Lenman 1959), and poliomyelitis (Pinelli & Buchthal 1951), but not, so far as I am aware, in peripheral neuropathy. The possible use of this fact as an electrodiagnostic test for the integrity of the motor nervre terminals has been suggested (Simpson 1960a, 1964). The nature of the abnormality of junctional transmission in myasthenia gravis and polymyositis is still uncertain. The safety factor of transmission could be reduced by a postjunctional abnormality of the endplate. Clinical and pharmacological studies do not permit a firm decision (Simpson 1960b). Nevertheless it is clear from this study of metabolic myopathy that the changes in myasthenia gravis and polymyositis cannot be accounted for by a postendplate lesion of muscle fibres and the balance of probability favours a pre-junctional mechanism in myasthenia gravis (Desmedt 1958, Elmqvist 1965). If this be accepted, one is driven to the conclusion that the myasthenic syndrome of polymyositis, and the recruitment effect described in that disease by Simpson & Lenman (1959) also point to a pre-junctional lesion. Have we discarded too readily the term 'neuromyositis'? This is of more than semantic importance for electromyography because it could imply a restoration of fibrillation to its former status as a pathognomonic sign of denervation. REFERENCES Buchthal F & Honcke P (1944) Acta med. scand. 116, 148 Desmedt J E (1958) Nature, Lond. 182, 1673 Eaton L M & Lambert E H (1957) J. Amer. med. Ass. 163, 1117 Elmqvist D (1965) Acta physiol. scand. 64, Suppl. 249, 1 Farmer T W, Buchthal F & Rosenfalck P (1960) Electroenceph. clin. Neurophysiol. 12, 455 Harvey A M & Masland R L (1941) Bull. Johns Hopk. Hosp. 69, 1 Hebb C 0 & Waites G M H (1956) J. Physiol. 132, 667 Hodes R (1948) Arch. Neurol. Psychiat., Chicago 60, 457 Lambert E H & Mulder D W (1957) Proc. Mayo Clin. 32, 441 Liley A W (1956) J. Physiol. 133, 571 Merton P A (1954) J. Physiol. 123, 553 Pinelli P (1957) Riv. Pat. nerv. ment. 78, 121 Pinelli P & Buchthal F (1951) Electroenceph. clin. Neurophysiol. 3, 497 Rooke E D, Eaton L M, Lambert E H & Hodgson C H (1960) Med. Clin. N. Amer. 44, 977 Simpson J A (1960a) In: Proc. R6un. Internat. d'informat. I1ectromyographique, Strasbourg (1960b) Scot. med.j. 5, 419 (1962) Develop. Med. child Neurol. 4, 55 (1964) Brit. med. J. ii, 709 Simpson J A & Lenman J A R (1959) Electroenceph. clin. Neurophysiol. 11, 604 Dr R G WilHlson (Institute of Neurology, London) Some Problems in the Diagnosis of Primary Muscle Disease The difficulty inherent in making accurate judgments of the degree of abnormality of the electromyogram recorded during voluntary effort is well known. From the figures given by Buchthal (1961) it seems likely that a concentric needle electrode of the type used in clinical diagnosis picks up potentials from motor units in the larger limb muscles of man during voluntary effort. These potentials will include spikes from units close to the needle tip and low voltage potentials from more distant units. For this
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