Journal ofNeurology, Neurosurgery, and Psychiatry 1995;59:629-632

SHORT REPORT

Eyelid "apraxia" in patients with motor neuron

disease

Kazuo Abe, Harutoshi Fujimura, Chikao Tatsumi, Keiko Toyooka, Shiro Yorifuji,Takehiko Yanagihara

AbstractThree patients with motor neuron dis-ease had eyelid "apraxia" with impairedvoluntary but preserved involuntary eye-lid movements. Attempts were made tolocalise the lesions responsible with neu-

roimaging and neuropathological exami-nation.

(_7NeurolNeurosurg Psychiatry 1995;59:629-632)

Keywords: motor neuron disease; eyelid apraxia;motor impersistence; ophthalmoparesis

Department ofNeurology, OsakaUniversity MedicalSchool, Osaka, JapanK AbeH FujimuraK ToyookaS YorifujiT YanagiharaDepartment ofInternal Medicine,Toyonaka MunicipalHospital, Toyonaka,JapanC TatsumiCorrespondence to:Dr Kazuo Abe, Departmentof Neurology, OsakaUniversity Medical School2-2 Yamadaoka, Suita,Osaka 565, Japan.Recieved 3 January 1995and in final revised form2 June 1995Accepted 7 July 1995

Oculomotor function is believed to be onlymarginally affected in patients with motorneuron disease.' Increasing evidence, how-ever, suggests that oculomotor dysfunctionmay actually occur more often than previ-ously thought.2- Eyelid movement has drawnlittle attention, even though damage to thecortico-oculomotor pathways or oculomotornuclei may cause abnormal eyelid move-

ments.5-9 We report three patients with motorneuron disease who had difficulty in volun-tary opening or closing of their eyelids andour attempts to localise the responsiblelesions by neuroimaging and neuropathalogi-cal examination.

All three patients were seen in our depart-ment at Osaka University between 1989 and1994, and clinically had both upper andlower motor neuron signs with bulbarinvolvement as well as neurogenic motor unitpotentials on EMG.10 All three underwentMRI and single photon emission computedtomography (SPECT) using technetium-99mhexamethyl propylene amine oxime (99mTcHMPAO). Neuropathological examinationwas subsequently carried out in two patients(1 and 2).

Case reportsPATIENT 1In 1991 a 69 year old right handed woman

noted an increasing difficulty in closing hereyes and it required a conscious and sus-

tained effort. She developed a habit of closingthe eyelids gently with her fingers, after whichthe eyes would remain shut. Her eyelidsremained closed normally during sleep. At

about the same time, she developed slurredspeech and difficulty in swallowing. Onexamination in 1991, she was alert and co-operative. Pupils were 3-5 mm and reacted tolight with normal convergence. She couldopen her eyes widely, and her voluntary ocu-lar movement and oculocephalic reflexes werenot impaired. Reflex blinking to bright light,visual threat, sudden noise, and corneal stim-ulation was normal. Spontaneous blinkingwas also present. She was unable to initiateclosure of her eyes voluntarily or on verbalcommand, although she comprehended whatwas requested. She could not improve herperformance by attempting to imitate theexaminer. Other commands, including open-ing or closing her mouth, protruding hertongue in any specific direction, and movingor turning her head, were carried out flaw-lessly. Her jaw jerk was brisk. There was mildweakness in the facial and tongue muscles.She had muscle atrophy, weakness, and fasci-culation in the upper limbs and shoulders.Deep tendon reflexes were slightly increasedin all extremities and Babinski's sign wasbilaterally positive. She had no extrapyrami-dal signs. Cognitive dysfunction was moder-ate on the mini mental state examination(MMSE) with a total score of 24; her failurewas in attention and recall, with preservedrecognition. She achieved only two categorieson the Wisconsin card sorting test (WCST).She had a normal score of 28 on Raven'scoloured progressive matrices (RCPM). AnECG was normal. An EMG showed motorunit potentials with high amplitude and longduration in the examined muscles includingthe facial and tongue muscles. Brain MRIdisclosed mild cerebral atrophy in the frontallobes and in the anterior part of the temporallobes (fig 1); SPECT showed reduced isotopeuptake in the frontal lobes and in the anteriorpart of the temporal lobes (fig 2). Her condi-tion steadily deteriorated with worsening ofdysarthria and dysphagia. She becamebedridden and died in 1993.

At necropsy, general pathology was unre-markable except for a lung abscess. The brainweighed 1100 g and showed diffuse corticalatrophy, more in the frontal lobes (fig 3).Microscopically, there were neuronal lossesand disarrangement of neuronal layers withcorticosubcortical astrocytosis which were

629 on S

eptember 10, 2020 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.59.6.629 on 1 D

ecember 1995. D

ownloaded from

Abe, Fujimura, Tatsumi, Toyooka, Yorfuji, Yanagihara

Figure 1 MRI with a 1 5Tesla superconductingsystem using a spin echomethod. T2 weightedimage (right), TR =

3000 ms, TE = 120 ms,showing mild atrophy inthe frontal lobes and in theanterior part of thetemporal lobes in patient 1.

-i

most severe in the precentral gyrus and mod-erate in the frontal region. There were nospongiform changes, neurofibrillary tangles,or senile plaques in the cortex. The deepwhite matter showed rarefaction of myelinsheaths with some periventricular collectionof lipid laden macrophages. The entire areaof the tegmentum of the pons and midbrainrelevant to oculomotor function was normal.Moderate neuronal loss with astrocytosis wasevident in the motor nuclei of the medullaoblongata and the anterior horn of the entirespinal cord. Degeneration of the pyramidaltract was traced from the spinal cord up tothe internal capsule and the corona radiata.There was no relevant lesion in other parts ofthe brain-including the basal ganglia andcerebellum-except for neuronal loss in thesubstantia nigra.

PATIENT 2A 64 year old right handed man noted

Figure 3 Coronal section of the left cerebral hemispherethrough the head of the caudate nucleus in patient 1.Cortical atrophy in the frontal lobe and diffuse palestaining of the deep white matter are evident (Kluver-Barrera stain).

dysarthria and muscle weakness in his rightupper arm and dysarthria in 1988. His weak-ness gradually worsened and spread to theleft upper arm and then to both lower limbs.In 1989, he began to be euphoric but, and atthe same time, began to have difficulty inopening his eyes after they were closed invol-untarily. At times, he could open his eyesonly by prising the lids apart with his fingers.On examination in 1989, he was alert andcooperative but laughed inappropriately.Pupils were 3 0 mm and reacted to light. Hehad full visual fields and full voluntary ocularmovements. Reflex blinking to bright light,visual threat, sudden noise, or corneal stimu-lation was normal. He had a blank facialexpression but spontaneous blinking was pre-sent. After closing his eyes he could not openthem for 20 to 30 seconds. Despite pro-nounced contraction of the frontal muscleswith the eyebrows well above the superiororbital rims, his eyes would remain closeduntil the upper lids were manually raised. Attimes, the patient opened his mouth to facili-tate eye opening. He had forced grasp andincreased jaw jerk. He had mild weakness inthe facial and tongue muscles. There wasmuscle atrophy in all extremities with fascicu-lation. Deep tendon reflexes were increasedin all extremities and Babinski's sign wasbilaterally positive. He had no extrapyramidalsigns. Cognitive dysfunction on MMSE wassevere, with a total score of 18; his failure wasin orientation, attention, and recall with pre-served recognition. He achieved only one cat-Figure 2 SPECT with 93-Tc HMPAO showing reduced isotope intake in the frontal

lobes in patient 1.

630 on S

eptember 10, 2020 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.59.6.629 on 1 D

ecember 1995. D

ownloaded from

Eyelid "apraxia" in patients with motor neuron disease

egory on WCST. He had a mildly impairedscore of 26 on RCPM, but he could fullyunderstand verbal commands. An EMGshowed motor unit potentials with highamplitude and long duration in the examinedmuscles including the facial and tongue mus-cles. Brain MRI disclosed mild cerebral atro-phy in the frontal lobes and the anterior partof the temporal lobes; SPECT showedreduced isotope uptake in the frontal lobesand the anterior part of the temporal lobes.His muscle weakness progressed further andhe died of bronchopneumonia in 1991.

At necropsy, general pathology was unre-markable except for the presence of broncho-pneumonia. The brain weighed 1030 g andshowed diffuse cortical atrophy, maximally inthe frontal lobes. Microscopically, corticalatrophy was the result of neuronal loss anddisarrangement of neuronal layers with cor-tico-subcortical astrocytosis, which were mostsevere in the precentral gyrus and moderatein the frontal region. There were no spongi-form changes, neurofibrillary tangles, orsenile plaques. The deep white mattershowed rarefaction of myelin sheaths withsome periventricular collection of lipid ladenmacrophages. The entire area of the tegmen-tum of the pons and midbrain relevant tooculomotor function was normal. In themotor nuclei of the medulla oblongata andthe anterior horn of the entire spinal cord,moderate neuronal loss with astrocytosis wasevident. Degeneration of the pyramidal tractwas traced from the spinal cord up to theinternal capsule and the corona radiata.There were no relevant lesions in other partsof the brain including the basal ganglia, sub-stantia nigra, and cerebellum.

PATIENT 3In 1993 a 68 year old right handed womanbegan to notice occasional difficulty in open-ing her eyes after they were closed involuntar-ily at bright light or visual threat.Subsequently, she noted dysarthria and dys-phagia. She also complained that she couldnot easily change her gaze from one object toanother. On examination in 1994, she wasalert and cooperative, but she laughed inap-propriately. Saccadic pursuit movements andslowing of ocular movement were present toall directions. She had normal primary eyeposition without limitation of involuntary eyemovements. She had no limitation in verticaloculocephalic reflex but Bell's phenomenonwas absent. After closing her eyes she couldnot open them for 20 to 30 seconds. Despitecontraction of the frontal muscles with eye-brows well above the superior orbital rims,the eyes would remain closed until the upperlids were manually raised. At times, thepatient opened her mouth to facilitate eyeopening. Reflex blinking to bright light, visualthreat, sudden noise, or corneal stimulationwas normal. She had forced grasp andincreased jaw jerk. She had mild weakness inthe facial and tongue muscles. Muscle atro-phy and fasciculation were present in alllimbs. Deep tendon reflexes were increased in

all limbs and Babinski's sign was bilaterallypositive. She had no extrapyramidal signs.Cognitive dysfunction on MMSE was moder-ate, with a total score of 23; her failure was inattention and recall and recognition was pre-served. She achieved only two categories onWCST. She had a normal score of 29 onRCPM. An EMG showed motor unit poten-tials with high amplitude and long duration inthe examined muscles including those of theface and tongue. A surface EMG showedcontraction in the frontal muscles but withoutcontraction of the orbicularis oculi muscleswhen she was ordered to open her eyes. Anelectrooculogram disclosed fixation instabilityaccompanied by square jerks, saccadic pur-suit movements, and slowing of occularmovement to all directions. Brain MRI dis-closed mild cerebral atrophy in the frontallobes and in the anterior part of the temporallobes. Reduced isotope uptake in the frontallobes and the anterior part of the temporallobes was shown by SPECT.

Discussion"Apraxia" of eyelid opening or closing hasbeen referred to as an inability to open orclose the eyes voluntarily despite normalorbicularis oculi muscles, preserved involun-tary opening or closing of eyes, alertness, andlanguage comprehension.7 All our patientscould keep their eyes open or closed oncethey could initiate eyelid movement. Thissuggests that eyelid apraxia may be a type ofan initiation failure of eyelid movements.Although we have used the term "apraxia" ofeyelid opening or closing in this report in theconventional way, the term "inability of initi-ating eyelid movement" may be more appro-priate.

Reported cases of "apraxia" of eyelid open-ing have been associated with extrapyramidaldiseases.578 On the other hand, apraxia ofeyelid closing has been discussed in relationto frontal lobe damage.6 Given these findings,most authors have distinguished "apraxia" ofeyelid opening from "apraxia" of eyelid clos-ing, but some have reported that both apraxiaof eyelid opening and apraxia of eyelid closingare caused by frontal lobe damage.56

It is noteworthy that all our patients had animpairment in attention and executive func-tion, the second of which is processed in thefrontal lobe.'1 The possibility of frontal lobeinvolvement was also supported by neu-roimaging and neuropathological examina-tion. Thus a selective loss of voluntary eyelidmovements with retention of the reflex activ-ity in our patients may derive from disease inthe frontal lobe or the frontopontine fibres.6Lapresle et al reported a patient with motorneuron disease with inability of voluntaryfacial movement including eyelid closing andsuggested dysfunction of the pyramidal tractas the cause of dissociation of voluntary con-trol and reflex ability.4 This is consistent withour findings.

Increasing evidence supports the fact thatpatients with motor neuron disease may

631 on S

eptember 10, 2020 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.59.6.629 on 1 D

ecember 1995. D

ownloaded from

Abe, Fujimura, Tatsumi, Toyooka, Yorzfuji, Yanagihara

develop frontal lobe dysfunction'2 13 and thatdamage to the frontal lobe caused by variousdiseases can affect eyelid movements.7-9Therefore, eyelid apraxia may occur inpatients with motor neuron disease, if the dis-ease process involves the frontal lobe.

1 Iwata M, Hirano A. Current problem in the pathology ofamyotrophic lateral sclerosis. In: Zimmermann H, ed.Progress in neurology. New York: Raven Press, 1979.

2 Lessell S. Supranuclear paralysis of voluntary lid closure.Arch Opthalmol 1972;88:241-4.

3 Harvey DG, Torack RM, Rosenbaum HE. Amyotrophiclateral sclerosis with ophthalmoplegia. A clinicopatho-logic study. Arch Neurol 1979;36:615-7.

4 Lapresle J, Salisachs P. Phenomenes de dissociationvolontaire et automatico-reflexe au niveau de certainsmuscles innerves par les paires craniennes dans deuxobservations de sclerose laterale amyotrophique. Revue

Neurologique 1976;132:157-61.5 Goldstein JE, Cogan DG. Apraxia of lid-opening. Arch

Ophthalmol 1965;3: 155-9.6 Nutt JG. Lid abnormalities secondary to cerebral hemi-

sphere lesions. Ann Neurol 1977;1:149-51.7 Dehaene I. Apraxia of eyelid opening in progressive

supranuclear palsy. Ann Neurol 1984;15:115-6.8 Lepore FE, Duvoisin RC. "Apraxia" of eyelid opening: an

involuntary levator inhibition. Neurology 1985;35:423-7.9 Johnston JC, Rosenbaum DM, Picone CM, Grotta JC.

Apraxia of eyelid opening secondary to right hemisphereinfarction. Ann Neurol 1989 25:622-4.

10 Li TM, Swash M, Alberman E, Day SJ. Diagnosis ofmotor neuron disease by neurologists: a study in threecountries. J Neurol Neurosurg Psychiatry 1991;54:980-4.

11 Heilman KM, Rothi LJG. Apraxia. In: Heilman KM,Valenstein E, eds. Clinical neuropsychology. Oxford:Oxford University Press, 1993:141-63.

12 Abe K, Fujimura H, Toyooka K, Hazama T, et al. Single-photon computed tomographic investigation of patientswith motor neuron disease. Neurology 1993;43:1569-73.

13 Kiernan JA, Hudson AJ. Frontal lobe atrophy in motorneuron diseases. Brain 1994;117:747-57.

HeadacheHeadaches seem to be an almost female prerogative inthe nineteenth century novel. None of Jane Austen'smen, not even the awful Mr Woodhouse, experiencethem. The symptom is often used by the sufferer,whether consciously or unconsciously, as a means ofavoiding a difficult social situation and afflicts, in JaneAusten's works, perhaps only the more fragile of hercreations. The robust Emma Woodhouse can hardlybe imagined falling back on such an expedient.Dickens, incidentally, hardly refers to any headachesufferers in his novels despite his experience of attacksof facial pain.'

Jane Austen, 1811, Sense and sensibilityMy sister will be equally sorry to miss the pleasure ofseeing you; but she has been very much plagued latelywith nervous head-aches, which make her unfit forcompany or conversation.

J7ane Austen, 1813, Pride and prejudiceThe agitation and tears which the subject occasioned,brought on a headache; and it grew so much worse

towards the evening that, added to her unwillingnessto see Mr Darcy, it determined her not to attend hercousins to Rosings, where they were engaged to drinktea.

Jane Austen, 1814, Mansfield Park"Fanny," said Edmund after looking at her attentively;"I am sure you have the headache?"

She could not deny it, but said it was not very bad"There was no help for it certainly," rejoined Mrs

Norris, in a rather softened voice; "but I question

whether her headache might not be caught then, sis-ter. There is nothing so likely to give it as standingand stooping in a hot sun. But I dare say it will be welltomorrow. Suppose you let her have your aromaticvinegar; I always forget to have mine filled."

Jane Austen, 1816, Emma"Miss Fairfax was not well enough to write;" andwhen Mr Perry called at Hartfield, the same morning,it appeared that she was so much indisposed as tohave been visited, though against her own consent, byhimself, and that she was suffering under severeheadaches, and a nervous fever to a degree, whichmade him doubt the possibility of her going to MrsSmallridge's at the time proposed.

Charlotte Bronte, 1839, Caroline Vernon"I've got a head-ache, Mary." This was a lie-told toawaken sympathy and elude further cross-examina-tion. "Have you, Adrian, where?" "I think I said ahead-ache, of course it would not be in my great toe."

Victor Hugo, 1862, Les MiserablesThis done, and saying that she had a headache,Cosette bade her father good night and went back toher bedroom ...Not that he was troubled by her headache, which

he regarded as nothing but a trifling crise de nerfs, agirlish sulk that would wear off in a day or two.

G D PERKINRegional Neurosciences Centre,

Charing Cross Hospital,Fulham Palace Road,London W6 8RF, UK

1 House M, Storey G, eds. The letters of Charles Dickens. Vol2. 1840-41. Oxford: The Clarenden Press, 1969.

NEUROLOGY IN LITERATURE

632 on S

eptember 10, 2020 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.59.6.629 on 1 D

ecember 1995. D

ownloaded from