British Journal of Ophthalmology 1996; 80: 350-355

Ocular neuromyotonia

Eric Ezra, David Spalton, Michael D Sanders, Elizabeth M Graham, Gordon T Plant

Medical Eye Unit, StThomas's Hospital,LondonE EzraD SpaltonM D SandersE M GrahamG T Plant

The National Hospitalfor NeurologicalDiseases, LondonM D SandersE M GrahamG T Plant

Correspondence to:Dr Gordon Plant, TheNational Hospital forNeurology andNeurosurgery, QueenSquare, London WC 1 3BG.

Accepted for publication21 December 1995

AbstractAims/Background-Ocular neuromyo-tonia is characterised by spontaneousspasm of extraocular muscles and hasbeen described in only 14 patients. Threefurther cases, two with unique features,are described, and the underlying mech-anism reviewed in the light of recentexperimental evidence implicating extra-cellular potassium concentration incausing spontaneous firing in normal anddemyelinated axons.Methods-Two patients had third nerveneuromyotonia, one due to compressionby an internal carotid artery aneurysm,which has not been reported previously,while the other followed irradiation of apituitary tumour, a common associationin the published reports. Selective activa-tion occurred in both, where neuro-myotonic activity was triggered byprolonged voluntary activation of specificextraocular muscles with or withoutspread of activity to other third nervemuscles. The other patient had fourthnerve involvement, where spasms of thesuperior oblique muscle were inducedonly by alcohol, a phenomenon which hasnot been described.Results-The two patients with thirdnerve involvement responded to carba-mazepine and in one, an improvement ina chronic partial third nerve paresisoccurred. The other has not requiredtreatment and remains asymptomatic byrefraining from alcohol.Conclusions-A careful examination,including the effects of prolonged volun-tary muscle action is required to initiateepisodes and to demonstrate selectiveactivation. Imaging is mandatory toexclude compressive intracranial lesions,particularly where there is no history ofpituitary fossa irradiation. A trial of anti-convulsants should be considered in allpatients. Extracellular potassium mayplay a role in spontaneous firing andephatic transmission in ocular neuro-myotonia.(BrJ Ophthalmol 1996; 80: 350-355)

In 1970 Ricker and Mertensl described apatient with idiopathic paroxysmal diplopia.During episodes, they noted a tonic unilateralesodeviation with restriction of elevation andabduction due to overaction of the medial andinferior rectus muscles. Papst2 in 1972described a similar patient with involvement ofthe medial, inferior and superior recti, and thelevator muscle. Electromyographic recordingsin both patients during quiescent periods

revealed a neurogenic pattern and they con-cluded that neuromyotonic activity resultedfrom spontaneous electrical activity in unstablemotor nerve membranes, followed by ephatictransmission of electrical activity to adjacentnerves, causing co-firing of different musclessupplied by the third nerve. This hypothesiswas supported by the fact that both patientsresponded and became asymptomatic aftertreatment with carbamazepine, an anticonvul-sant. The term 'ocular neuromyotonia' wasused to describe the syndrome. Further reportsin the literature have been sparse3-6 as sum-marised in Table 1.The condition is distinct from superior

oblique myokymia, which is characterised byoscillopsia and microtremor due to phasicrather than tonic activity.7 8 It is also distinctfrom cyclical oculomotor spasm, which occursin the setting of a congenital third nerve pare-sis, where cycles have characteristic pupillaryinvolvement without tonic adduction.9Although surgery or, more specifically, irradia-tion for pituitary fossa and other intracranialtumours is the usual aetiology, ocular neuro-mytonia may occur with other intracranialcompressive lesions, or in the absence of anycausative factors.1-5 Any of the ocular motornerves may be affected, often in the setting of achronic nerve paresis and episodes may beelicited by sustained activity of the extraocularmuscle supplied by the nerve involved or mayoccur spontaneously. 1-6The diagnosis may be easily overlooked in a

patient complaining of paroxysmal diplopiabecause a careful examination of ocular motil-ity, including the effects of sustained action ofindividual muscles, is required. Furthermore,effective treatment with anticonvulsants isavailable. Our experience suggests that wherethe cause is not clear (particularly if there is noprevious history of radiation therapy) allpatients should be investigated for intracranialdisease.These points are illustrated with a descrip-

tion of three further cases.

Methods and patientsThe three patients in this study were allreferred following an initial examination bytheir ophthalmologist. All patients had a fullophthalmic, neurological, and general exami-nation. Ophthalmic examination includedcareful assessment of ocular motility, with par-ticular attention to the following:

(1) Ocular motility during quiescent peri-ods, with careful documentation of chronicnerve pareses, including signs of oculomotorsynkinesis ('aberrant regeneration') in thirdnerve involvement. A Hess examination wasperformed on all patients. Pupillary synkinesis

350

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from

Ocular neuromyotonia

Table 1 Summary of the 17 cases of ocular neuromyotonia in the literature

Chronic palsyl Neuromyotonic muscle Treatment TreatmentCase Radiation Time to aberrant involvement (and response response (chronicAge/sex Aetiology (Gy) onset Nerve regeneration triggering muscles) (symptoms) nerve palsy)

Ricker and Mertens'1 Nil Nil III Nil MR, IR Full resolution

Papst22 Nil Nil III Nil MR, IR, SR, LP Full resolution

Shults et al33 Pituitary adenoma, 75 9 Months III AR lid only MR, IR, SR, LP, P Full resolution Full resolution60M craniotomy (triggered by MR, IR)4 Pituitary adenoma, 45-6 7 Years III Partial III MR, IR, SR, LP No response No response62F craniotomy AR lid (triggered by MR, IR)5 Pituitary adenoma, 50 4 3 Years III AR lid only MR, IR, SR, LP Partial response ?52M TSA6 Nil Nil - III AR lid only MR, IR, SR, LP Partial response Full resolution74F (triggered by IR)7 Nil Nil - IV Nil SO ? ?12M8 Pituitary adenoma, 66 3 Years VI Nil LR (triggered by LR) No response46M craniotomy

Lessell et a149 Craniopharyngioma, 50 05 2 Years III Nil SR? ? ?19F craniotomy10 Pit adenoma, TSA 54 11 Months III Nil MR ? ?17F11 Skull base sarcoma 70-2 2 Months VI Partial VI LR ? ?51F (no surgery)12 Skull base 40 4 Years VI Nil LR No treatment,1IF rhabdomyosarcoma partial resolution

Salmon et al513 Pituitary adenoma, 45 7 Years III Nil IR, SR, LP Full resolution36F TSA

Barroso and Hoyt614 Thalamic glioma (no 77 16 Months VI Nil LR (triggered by LR) No treatment, full7M surgery) resolution

Ezra et al (this study)15 Internal carotid Nil - III Partial III MR, LP (triggered by Partial response Unchanged60M aneurysm MR, LP)16 Pituitary adenoma, 36 9 Years III Partial III MR, IR, SR, LP, P Partial response Partial44M craniotomy AR (triggered by MR, IR) improvement17 Nil Nil - IV Nil SO No treatment,40M unchanged

TSA=trans-sphenoidal adenohypophysectomy, AR=aberrant regeneration, MR=medial rectus, IR=inferior rectus, SR=superior rectus, LR=lateral rectus,SO=superior oblique, LP=levator palpebrae, P=pupillomotor, ?=unknown.

(case 2) was confirmed by pupillometry. Upperlid position and retraction on downgaze, a signof upper lid synkinesis, were recorded.

(2) Episodes of neuromyotonic spasmswere induced by prolonged voluntary activityof individual extraocular muscles in turn. Eachmuscle was tested to determine whether itcould act as the triggering muscle.

(3) During neuromyotonic episodes the fol-lowing were recorded: (i) duration and symp-toms, particularly the nature of the diplopia;(ii) which muscles were co-firing - this couldbe determined by ocular deviation in all posi-tions of gaze and by eliciting mechanicalrestriction of the antagonists; (iii) upper lidposition in primary gaze and the effects ofdowngaze, which accentuates any spasm ofthe levator palpebrae; (iv) pupillary spasm;(v) globe retraction due to co-firing of extra-ocular muscles; (vi) the presence of torsionaldiplopia, intorsion, and hypodeviation weretaken as a sign of superior oblique spasm (case3) and microtremor was sought by slit-lampexamination.

(4) In case 3, episodes could not be elicitedduring several examinations. The patient wastherefore asked to drink approximately 100 mlof spirit in order to allow observation of anepisode.

All patients underwent computed tomogra-phy (CT) or magnetic resonance imaging(MRI) with contrast, and MRI cerebral vesselangiography was performed to confirm sus-pected vascular lesions (case 1). All patientsalso had neurological examination, includingfull blood screening. An edrophonium

(Tensilon) test to exclude myasthenia gravis,was performed in all patients, where an intra-venous injection during a quiescent period wasfollowed by a careful examination of ocularmotility to determine whether edrophoniumcould abolish neuromyotonic triggering.

Results

CASE 1A 60-year-old man was referred with a 1 yearhistory of right supraorbital pain. The familyhad noted that, from time to time, his right eyewould appear to stare. Direct questioningrevealed episodes of intermittent diplopia, withvariable horizontal and vertical componentsand no precipitating factors of which thepatient was aware. He also had a history ofhypertension, ischaemic heart disease, andperipheral vascular disease. Alcohol consump-tion had been high, in excess of 40 units perweek for several years, though episodes werenot related to alcohol consumption. Neuro-ophthalmic examination showed a partial rightthird nerve palsy and signs of oculomotor syn-kinesis, with upper lid retraction on downgaze(Fig 1 A-C) and pupillary synkinesis. Theright corneal reflex was reduced but there wereno other abnormal neuro-ophthalmic orneurological signs. Systemic examinationrevealed bilateral carotid bruits and hyperten-sion but was otherwise unremarkable.

Sustained elevation of the right eye resultedin paroxysmal spasm of the right levatormuscle, the upper lid becoming markedly

351

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from

Ezra, Spalton, Sanders, Graham, Plant

Figure I Case 1. (A-C)A partial chronic right thirdnerve paresis is presentduring quiescent periods,with a right hypotropia andptosis (A), right upper lidretraction on downgaze (B)and weakness of rightelevation (C).(C-E) Right levatorneuromyotonia. Onsustained upgaze (C),levator spasm is induced,resulting in increased upperlid retraction, particularlyon downgaze (D, E).(F-I) Right medial rectusneuromyotonia. Duringquiescent periods, rightlateral gaze is full (F).Sustained left gaze (G)induces right medial rectusneuromyotonia withrestriction of right lateralrectus action (H). Withresolution of the episode,full abduction of the righteye is restored (I).Simultaneousneuromyotonia of thesuperior rectus/levatorcomplex and the medialrectus could not be elicited.

U

E

retracted, particularly on attempted downgaze(Fig 1 C-E). Ocular motility and pupillaryresponses remained unchanged during theseepisodes. A different pattern of activity couldbe provoked by sustained adduction of theright eye. During these episodes, paroxysmalspasm of the medial rectus would occur, withrestriction of abduction, and unaffected lidposition (Fig 1 F-I). Both types of episodestypically lasted between 2 and 3 minutes. Theclinical pattern reflected levator and medialrectus involvement, although simultaneousoveraction of these could not be elicited in asingle episode and co-firing of other musclessupplied by the third nerve did not occur. Bothtypes of episodes could be easily reproduced.A Ti MRI scan revealed a supraclinoid

mass on the right, with a mixed signal sug-gestive of a partially thrombosed aneurysm(Fig 2). This was confirmed by MRI angio-graphy which showed an aneurysm of theinternal carotid artery at its junction with theposterior communicating artery, impinging onthe roof of the right cavernous sinus where thethird nerve enters the sinus (Fig 3). Treatmentwith carbamazepine 200 mg twice dailyresulted in full resolution of symptoms within aweek, but the partial third nerve paresisremained unchanged. An attempt to reducethe dosage resulted in recurrence of symptomsand the original dose was recommenced. Hehas had no further attacks on treatment after1 year.

CASE 2A 44-year-old man with headache, right visualdisturbance and gynaecomastia was found tohave visual acuities of 6/12 right and 6/6 left,with a bitemporal hemianopia, a right central

scotoma, and right optic disc pallor and afferentpupillary defect, suggesting anterior chiasmalcompression. Ocular motility and neurologicalexaminations were unremarkable and generalexamination revealed signs of panhypopitu-itarism. A CT scan confirmed the presence of alarge pituitary fossa mass with suprasellarextension, and a markedly raised serum pro-lactin indicated a prolactinoma. At the time,bromocriptine therapy was not available andhe underwent a frontal craniotomy andhypophysectomy, followed by postoperativeirradiation with 36 Gy. Thereafter, heremained well on endocrine replacement ther-apy and showed improvement in visual fieldsand acuity of the right eye.Nine years later he presented with episodes

of paroxysmal vertical and horizontal diplopia,associated with a 'pulling' sensation in theright eye usually occurring while driving longdistances and looking in the rear mirror orwhen tired or under extreme stress. Duringthese episodes he invariably noted that theright eye would 'stare'. Typically, episodeswould last between seconds and minutes andresolve spontaneously, with several occurringover a period of several hours. At the time,ocular motility and eyelids were reported asnormal, though the effects of sustained muscleactivity were not sought. Visual field and CTexamination on three occasions failed to showany change or tumour recurrence. Over thenext 3 years, episodes became increasinglyfrequent, to the extent that he was no longerable to drive without symptoms. He also devel-oped a mild chronic third nerve paresis, a2 mm ptosis, pupillary dilatation, and oculo-motor synkinesis (aberrant regeneration),with lid retraction on downgaze and pupillarysynkinesis confirmed by pupillometry.

352

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from

Ocular neuromyotonia

Figure 2 Case 1. Magnetic resonance imaging scanshowing a mixed signal lesion impinging on the roofof thecavernous sinus posteriorly (arrow).

Figure 3 Case 1. Magnetic resonance cerebralangiography showing the lesion to be a partially thrombosedaneurysm (arrow).

Attacks could be provoked by sustainedadduction and depression of the right eye.During episodes, the right eye would becometonically deviated in adduction, with restric-tion of all ocular movements, particularlyabduction and elevation, and marked upper lidretraction due to levator overaction. In addi-tion pupillary involvement would occur, thepupil becoming fixed in partial miosis, failingto react to light or accommodation. Thepatient reported vertical and horizontal

t~~~~~~~~~~~~~~~.'-

Itt.,*1' es

(7m-z- btco Wr ct

Left E.r

Figure 4 Case 2. Hess charts comparing basal third nerve function before (above) andafter (below) treatment with carbamazepine. After treatment, marked improvement inthird nemve function occurred, though mild weakness in elevation of the right eye persists.

diplopia, without torsion, during these attacks,which lasted a variable period from seconds tominutes. The clinical pattern thereforereflected co-firing of pupillomotor, levator andmedial, inferior and superior rectus musclefibres, triggered by sustained voluntary activityof the medial and inferior recti.

Treatment with carbamazepine 200 mgtwice daily resulted in a dramatic improvementof symptoms within a week. In addition, thechronic third nerve paresis improved markedly(Fig 4), with only mild limitation of upgaze,and mild upper lid retraction on downgazeremaining after 2 months of treatment.Although he reported occasional symptoms ontreatment, no further attacks could be elicited.

CASE 3A 40-year-old man was referred with a 4 yearhistory of paroxysmal vertical diplopia.Episodes typically lasted between 10 and 20seconds and would occur repetitively aftermoderate to high alcohol consumption. He didnot report any oscillopsia or eyelid abnormali-ties during attacks. No relevant medical historywas elicited.

Neuro-ophthalmic and neurological exami-nation proved unremarkable initially, but afterconsumption of about 100 ml of spirit underobservation, a series of attacks occurred overthe space of 20 minutes. During episodes,which occurred spontaneously and indepen-dently of eye position, he would develop a righthypotropia due to superior oblique overactionwith torsional and vertical diplopia. No oscil-lopsia or microtremor occurred and eyelidposition and pupillary reactions remainednormal throughout. Each episode wasextremely short lived, thereby precluding amore detailed examination. Activity could notbe induced in the absence of alcohol.MRI studies failed to reveal any intracranial

abnormality and an edrophonium test during

353

f-.p"

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from

Ezra, Spalton, Sanders, Graham, Plant

an episode proved negative. He did not receivetreatment and remains asymptomatic if heabstains from alcohol.

DiscussionAll 17 cases of ocular neuromyotonia in theliterature,'-6including the three reported here,are summarised in Table 1. Eleven hadintracranial tumours treated with surgeryand/or radiotherapy, the period between treat-ment and onset of symptoms ranging from 2months to 9 years. Four patients had no iden-tifiable cause and two associations are reportedhere for the first time - oculomotor nerve com-pression (case 1) and an association withalcohol consumption (case 3). Case 1 in ourseries is the first patient with ocular neuro-myotonia to be described in association with acompressive lesion. However, the patientdescribed by Bateman and Saunders,'0 apatient with a supraclinoid aneurysm, achronic third nerve paresis with synkinesis, andparoxysmal third nerve spasm was interpretedas having a cyclical oculomotor palsy but maywell have been a case of ocular neuromyotonia,as has been suggested by previous authors.3

Eleven patients had involvement of the thirdnerve, two of the fourth nerve, and four of thesixth nerve. Ten patients in total received anti-convulsant therapy, eight showing a reductionin the frequency of symptoms. Perhaps moreremarkably, three patients, our case 2 and twopatients described by Shults et al,3 showedimprovement of chronic nerve paresis on treat-ment. Of the 11 patients with third nerveinvolvement, six had evidence of a chronicnerve paresis with signs of oculomotor syn-kinesis and five had normal ocular motilityduring quiescent periods. eight had levatorinvolvement, nine medial rectus, eight superiorrectus, and eight inferior rectus involvementduring episodes. Only two patients had pupil-lary involvement.

In the two patients we have described withthird nerve neuromyotonia, the phenomenonof selective activation occurred, that is to saysustained action of certain muscles provokedthe spasms. This was also described in four ofthe six patients in the series of Shults et al,3with activation most commonly occurringthrough action of the medial and inferior recti.In case 2 medial and inferior rectus overactionresulted in co-firing of the other muscles. Case1 showed two quite distinct patterns of neuro-myotonic activity, where sustained upgazetriggered overaction of the levator and activityof the medial rectus triggered overaction ofthat muscle only. Activity did not 'spread' fromthe medial rectus to the levator or vice versa.This pattern has not been previously reportedand some degree of co-activation is the rule.

Ocular neuromyotonia of the fourth nervehas only been described in two patients,including case 3 in our series, and typicallyinvolves spontaneous superior oblique over-action without microtremor or oscillopsia,reflecting the tonic, rather than phasic,nature of the neural discharges in neuromyo-tonia. This patient is the only case of ocular

neuromyotonia provoked by alcohol. The casedescribed by Clark" as superior oblique over-action without oscillopsia or microtremor, wasprobably the first case of fourth nerve neuro-myotonia to be described in the literature, ashas been pointed out by previous authors.3As a clinical syndrome, fourth nerve neuro-

myotonia may be differentiated from superioroblique myokymia. In addition to a hypo-tropia, the symptom of oscillopsia, in associa-tion with microtremor and intorsion, which arebest observed by slit-lamp examination, istypical of myokymia and reflects phasic neuralactivity rather than the tonic activity seen inneuromyotonia. However, both conditionsmay represent a spectrum of disease with acommon underlying mechanism, with the dis-tinction being purely clinical.

Sixth nerve neuromyotonia has beendescribed in four patients. It involves intermit-tent exotropia with restriction of adduction,and is triggered by sustained action of thelateral rectus muscle. The patient described byBarroso and Hoyt6 is unique in that this is theonly reported case where resolution of neuro-myotonia occurred spontaneously withoutanticonvulsant therapy. Metz and Sterns'2described a woman with a chronic sixth nerveparesis, following pituitary surgery and irradia-tion, who developed 'variable esotropia-exotropia'. The clinical picture would beconsistent with sixth nerve neuromyotonia.

In ocular neuromyotonia the spasm resultsfrom spontaneous neural firing in a singleneuron or a group of neurons supplying theactivating muscle or muscles. Interneuraltransmission to other neurons supplying thesame or other muscles may then occur result-ing in a self perpetuating circuit.13 This wouldexplain 'selective activation' by specificmuscles and subsequent co-firing of othermuscles in third nerve neuromyotonia andtonic activity in fourth and sixth nerve involve-ment.

Support for this mechanism has come fromevidence in other neurological conditions suchas radiation plexopathy,13 peripheral neuro-pathy,14 15 traumatic neuropathy,16 and hemi-facial spasm,'7 where spontaneous firing hasbeen shown to occur in segmentally demy-elinated axons. Patients with limb myokymiadue to radiation plexopathy exhibit similarelectromyographic activity to those with ocularneuromyotonia. 13

In experimental models, spontaneous firingin demyelinated axons has been demonstratedin rat spinal root axons,18 cat dorsal columns,'9and rat trigeminal nerve.20 Ectopic actionpotentials also occur in normal, myelinatedmammalian axons where extracellular potas-sium concentration has been elevated2l includ-ing following sustained tetanic activation.22 Inocular neuromyotonia, therefore, it is possiblethat damaged axons become susceptible tospontaneous firing. Extracellular potassiummay be elevated when axons are subjected tosustained activity, thus explaining the trigger-ing that occurs with sustained muscle activity.For co-firing of neurons supplying othermuscles to be initiated interneural electrical

354

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from

Ocular neuromyotonia

transmission must occur; perhaps this may alsooccur as a result of changes in extracellularpotassium.

In oculomotor synkinesis, it has previouslybeen argued that aberrant regeneration oraxonal misdirection may not account for co-firing. Two alternative mechanisms have beenproposed.23 The first is ephaptic (lateral)transmission between axons and the secondinvolves central synaptic reorganisation follow-ing injury. As most patients with third nerveneuromyotonia also show signs of synkinesisduring quiescent periods ephaptic transmis-sion may be relevant to both phenomena. Thismay account for the disappearance of syn-kinesis in case 2 following anticonvulsanttherapy - its disappearance has also beendescribed following treatment of a lymphomacausing oculomotor nerve synkinesis.24 Itwould be difficult to explain these observationsif the synkinesis were due to a 'hard wired'aberrant regeneration.The role of alcohol consumption in precipi-

tating attacks in patient 3 is unknown. Studiesexamining the effects of alcohol on humanperipheral nerve function have not shownsimilar effects in peripheral nerves.25-27Finally, the marked improvement in basalnerve function with anticonvulsant treatmentin case 2 and in the two other patientsdescribed in the literature,3 implies thatchronic paresis is at least in part due to nervemembrane instability. The improvement ofsuch a paresis may have wider implications forthe treatment of other peripheral and centralneuropathies and demyelinating disorders.We are grateful to Dr Raju Kapoor for his contribution to thediscussion and to the orthoptic department at St Thomas'sHospital for their contributions.

1 Ricker VK, Mertens HG. Okulare Neuromyotonie. KinMonatsblAugenheilkd 1970; 156: 837-42.

2 Papst W. Zur differentialdiagnose der okularen neuro-myotonie. Ophthalmologica 1972; 164: 252-63.

3 Shults WT, Hoyt WF, Behrens M, Maclean J, Saul RF,

Corbett JJ. Ocular neyromyotonia. A clinical descriptionof six cases. Arch Ophthalmol 1986; 104: 1028-34.

4 Lessell S, Lessell IM, Rizzo JF. Ocular neuromyotonia afterradiation therapy. Am J Ophthalmol 1986; 102: 766-70.

5 Salmon JF, Steven P, Abrahamson MJ. Ocular neuro-myotonia. Neuro-ophthalmol 1988; 4: 181-5.

6 Barroso L, Hoyt WF. Episodic exotropia from lateral rectusneuromyotonia - Appearance and remission after radia-tion therapy for a thalamic glioma. J7 Paediatr OphthalmolStrabismus 1993; 30: 56-7.

7 Rosenberg ML, GlaserJS. Superior oblique myokymia. AnnNeurol 1983; 13: 667-9.

8 Lee JP. Superior oblique myokymia: a possible aetiologicalfactor. Arch Ophthalmol 1984; 102: 1178-9.

9 Lowenfeld IE, Thompson HS. Oculomotor paresis withcyclical spasms: a critical review of the literature and anew case. Surv Ophthalmol 1975; 20: 81-124.

10 Bateman DE, Saunders M. Cyclic oculomotor palsy.Description of a case and hypothesis of the mechanism.J Neurol Neurosurg Psychiatry 1983; 46: 451-4.

11 Clark E. A case of apparent intermittent overaction of thesuperior oblique. Br OrthopticsJ1 1966; 23: 116-7.

12 Metz HS, Stems G. Varying esotropia-exotropia. Y PaediatrOphthalmol Strabismus 1985; 22: 97-9.

13 Albers JW, Allen AA, Bastron JA, Daube JR. Limbmyokymia. Musde Nerve 1981; 4: 494-504.

14 Lance JW, Burke D, Pollard J. Hyperexcitability of motorand sensory neurons in neuromyotonia. Ann Neurol 1979;5: 523-32.

15 Warmolts JR, Mendell JR. Neurotonia: impulse inducedrepetitive discharges in motor nerves in peripheralneuropathy. Ann Neurol 1980; 7: 245-50.

16 Stohr M. Repetitive impulse induced EMG discharges inneuromuscular disease. Ann Neurol 1981; 9: 204-10.

17 Nielsen VK. Pathophysiology of hemifacial spasm: I.Ephatic transmission and ectopic excitation. Neurology1984; 34: 418-26.

18 Baker M, Bostock H. Ectopic activity in demyelinatedspinal root axons of the rat. J Physiol 1992; 451: 539-52.

19 Smith KJ, Macdonald WI. Spontaneous and evoked electri-cal discharges from a central demyelinating lesion.JNeurol Sci 1982; 55: 39-47.

20 Buchiel KJ. Abnormal impulse generation in focallydemyelinated trigeminal roots. J Neurosurg 1980; 53:647-83.

21 Kapoor R, Smith KJ, Felts PA, Davies M. Internodal potas-sium currents can generate ectopic in mammalian myeli-nated axons. Brain Res 1993; 611: 165-9.

22 Bostock H, Bergmans J. Post-tetanic excitability changesand ectopic discharges in a human motor axon. Brain1994; 117: 913-28.

23 Lepore FE, Glaser JS. Misdirection revisited. A criticalappraisal of acquired oculomotor nerve synkinesis.Arch Ophthalmol 1980; 98: 2206-9.

24 Sze HL, Yew KY, Chai BT, Tjia H. Transient oculomotornerve synkinesis in non-Hodgkin's lymphoma. J ClinNeuro-ophthalmol 1992; 12: 203-6.

25 Letz R, Gerr F. Covariates of human peripheral nervefunction: I. Nerve conduction velocity and amplitude.Neurotoxicol Teratol 1994; 16: 95-104.

26 Letz R, Gerr F. Covariates ofhuman peripheral nerve func-tion: II. Vibrotactile and thermal thresholds. NeurotoxicolTeratol 1994; 16: 105-12.

27 Letz R, Gerr F. Covariates of human peripheral nerve func-tion: III. Effects of reported drinking. Neurotoxicol Teratol1994; 16: 113-22.

355

on Decem

ber 25, 2019 by guest. Protected by copyright.

http://bjo.bmj.com

/B

r J Ophthalm

ol: first published as 10.1136/bjo.80.4.350 on 1 April 1996. D

ownloaded from