Some neuro-ophthalmological observations' · This paper records some neuro-ophthalmological observations made on the Stroke Service of the Massachusetts General Hospital. For the

J. Neurol. Neurosurg. Psychiat., 1967, 30, 383

Some neuro-ophthalmological observations'C. MILLER FISHER

From the Neurology Service of the Massachusetts General Hospital and theDepartment of Neurology, Harvard Medical School

This paper records some neuro-ophthalmologicalobservations made on the Stroke Service of theMassachusetts General Hospital. For the most partthey are not mentioned in textbooks of neurology.Although they are but minor additions to theclinician's fund of knowledge, their recognition mayaid in accurate diagnosis. Some are possibly ofinterest in their own right as illustrations of theintegrated action of the central nervous system.Since the abnormalities are generally unrelated, theywill be discussed individually.

DILUTED PUPIL IN OCCLUSION OF THE INTERNALCAROTID ARTERY

Several times, in occlusion of the internal carotidartery we have found the ipsilateral pupil enlargedand fixed or poorly reactive to light.

A man, aged 69, with bilateral internal carotid arteryocclusion had two spells of unconsciousness six monthsand five months before admission. The first lasted fiveminutes, the second, 20 seconds. There were no residualill effects. A short time later it was found that the rightpupil was larger than the left (right 7 mm., left 3 mm.)and that the right pupil reacted sluggishly to light directlyand consensually. The extraocular movements were full.There was no ptosis. Sweating on the forehead was notdifferent on the two sides.The central retinal artery diastolic pressure was

approximately 20 units in each eye. Arteriographyshowed bilateral internal carotid artery occlusion withextensive filling of the carotid territory intracranially viathe ophthalmic arteries. A vertebral angiogram showedfilling of the carotid system from the basilar artery.

Extensive neovascularization of the retina was presentbilaterally. Gonioscopy demonstrated a confluent densemesh of fine vessels involving the iris of the right eye overa 3600 extent and a slight involvement of the left iris. Adiagnosis of rubeosis iridis was made. Glaucoma was notpresent and there was no cataract formation. Atrophy ofthe iris was not described.A glucose tolerance curve showed a fasting blood sugar

'This study was aided by grant no. NB-05 152 of the National Instituteof Neurological Diseases and Blindness, U.S.P.H.S. This paper waspresented at a seminar at the Massachusetts Eye and Ear Infirmary,22 December 1966.

of 76, half hour 150, one hour 180, two hours 147 mg. 00The blood cholesterol was 383 mg. %.A diabetic man, age 49, had noted three months before

admission that vision in the right eye was 'broken into ajig-saw puzzle'. Everything looked gray and he saw onlyfragments of objects here and there; e.g., in looking ata face he saw part of an eye and a little of the mouth. Onemonth before admission vision had become worse and hecould see only from the corner of the right eye. Fourmonths before admission at a time when vision wasintact, it had been noted that the right pupil was dilatedand unreactive.

Pulsation was absent on the right side in the upperextremity and in the subclavian, common carotid,external carotid, and temporal arteries, i.e., distal to theinnominate artery. The right pupil was 6 mm., slightlyirregular and fixed. The left pupil was 3 mm. and reactive.The retina of the right eye presented a most unusualpicture, a slow movement of blood being visible in almostall veins. The arteries were attenuated and the optic discwas pale. The central retinal artery pressure on the rightwas virtually zero, on the left, 65, diastolic. The extra-ocular movements were full and there was no ptosis.Vision was limited to a small sector of the inferiortemporal visual field. There was early neovascularizationof the iris, especially at the angle. A diagnosis of earlyrubeosis iridis was made. Dr. J. B. Whitney, whoperformed the ophthalmological examination, attributedthe mydriasis to atrophy of the iris.

In another case, a man aged 50 with a mild righthemiparesis and dysarthria, bilateral occlusion of theinternal carotid arteries was found. The left pupil was6 mm. and reacted poorly, the right was 4 mm. andreacted well.

In these cases the lack of associated neurologicalsymptoms suggests that the mydriasis is the resultof a local disorder of the iris, probably ischaemicatrophy rather than a primary nervous derangement.The abnormality has been described in the past inTakayasu's disease in which the carotid circulationis obliterated by an arteritic process (Walsh, 1957).

OCULAR SIGNS IN LARGE HYPERTENSIVEINTRACEREBRAL HAEMORRHAGE

Hypertensive haemorrhage has four main sites ofpredilection: putamen 60%, thalamus 10%, pons

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10%, and cerebellum 10%. Ocular signs are all-important in identifying the site of the bleeding andhelping to determine the feasibility of surgery. Thesesigns may be pithily summed up as follows:

In putaminal haemorrhage there is a hemiparesisand the eyes are deviated conjugately to the oppositeside. In thalamic haemorrhage there may be ahemiparesis and the eyes are deviated downwards asif peering at the nose. Vertical eye movements areimpaired and the pupils are about 2 mm. in size andunreactive. In pontine haemorrhage the eyes are inthe central position, the pupils are pin point andreactive, reflex eye movements are absent, and ocularbobbing may be present. In cerebellar haemorrhagethere is a forced conjugate lateral deviation of theeyes, a paralysis of conjugate lateral gaze, or a sixthnerve palsy without paralysis of the limbs. Thepupils are of average size and reactive.

PRESERVATION OF THE PUPILLARY REACTION INPONTINE MIOSIS

One of the classical diagnostic signs of intrapontinehaemorrhage or massive pontine infarction has beensmall (1 mm.) fixed pupils. The cause of the miosis iscustomarily held to be interruption of the descendingsympathetic pupillo-dilator fibres, but the mechanismof failure of the pupils to react to light has remainedunexplained.We have carefully tested the reaction of pinpoint

pupils in four patients with pontine haemorrhage andtwo with massive pontine infarction. Using a brightlight and a hand lens, it was possible in each case toobserve a definite reaction. Extreme miosis hasprobably caused the reaction to be overlooked inthe past. This finding relieves the neurologist oftrying to explain how a pontine lesion paralyzes thepupillary reaction.While on this subject it may be added that pontine

miosis has not been encountered as a unilateralphenomenon and probably occurs only with bilateralinterruption of the descending sympathetic system.

CONJUGATE DEVIATION OF THE EYES TO THE 'WRONG'SIDE IN SUPRATENTORIAL HAEMORRHAGE

It is axiomatic that a large supratentorial haemor-rhage causes a contralateral hemiplegia and deviationof the eyes away from the paralyzed side, towardsthe side of the lesion. In occasional cases, however,most signs point to a supratentorial haemorrhagewhen the eyes are tonically deviated conjugately tothe side of the hemiplegia mimicking the formula ofa pontine lesion.

In three successive such cases the haemorrhage onpathological examination has proved to be located

in the medial part of the thalamus on one side witha relatively massive collection of blood within thethird ventricle.

In one case an 89-year-old hypertensive woman wasadmitted with a right hemiparesis and forced conjugatedeviation of the eyes to the right and downwards. Thepupils were 4 mm. and unreactive. Necropsy showed a2 cm. haemorrhage lying in the left mid-thalamus extend-ing into and distending the third ventricle. There werescattered ancient softenings in the right occipital lobe dueto an old occlusion of the right posterior cerebral artery.There was also a cavity 2 by 5 mm. in the anterior limb ofthe internal capsule on the right side and a 1 mm. 'lacune'in the mid-pons.

In another case a hypertensive man aged 49 wasbrought to the emergency ward having collapsed 30minutes before. He was restless, moving the right sideaimlessly. The left arm was tonically flexed, the left legtonically extended. The pupils were 2 mm. in diameterand unreactive to light. The head and eyes turned spas-modically to the left. The eyes did not move to the righton head rotation. The patient died 12 hours later.Pathological examination showed a large haemorrhageinto the thalamus on the right side with blood ballooningthe third ventricle, and, in addition, blood had dissecteddownwards into the midbrain and pons. The absence ofsuch a dissection in the first case indicates that thisdownward tracking is not a necessary part of the process.The third patient had a left hemiplegia, non-reactivepupils and roving movements of the eyes from the centralposition fully to the left but not to the right. Pathologicalexamination was much the same as in the case justdescribed.

PUPILLARY SIZE IN BRAIN STEM LESIONS

Studies of the effect of brain stem lesions at variouslevels on pupillary size have led to the followingconclusions: (1) lesions located in the subthalamusproduce a moderate miosis (2-3 mm. approximately);(2) subtotal damage to the midbrain as in tentorialhemiation produces huge pupils (7-10 mm.) pre-sumably due to paralysis of the parasympatheticoutflow; (3) with more extensive midbrain damagethe pupils are less widely dilated (4-6 mm.)presumably because the sympathetic fibres passingdownwards are also interrupted; (4) a large lesion ofthe tegmentum of the pons produces an intensepinpoint miosis (I mm.) which is usually attributedto sympathetic paralysis and sparing of the para-sympathetics; (5) combined pontine-midbrain dam-age results in a pupil of the same size as in (3), i.e.,intermediate in size between (2) and (4), para-sympathetic interruption being added to pontinesympathetic paralysis. The failure of the pupil to beof pinpoint size with total cervical cord lesions and inHomer's syndrome has not yet been explained.

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Some neuro-ophthalmological observations

REFLEX EYE MOVEMENTS IN COMA

It is now routine neurological practice in cases ofcoma to determine the reflex eye movements on headrotation and on ice water irrigation of the ear canals.When necessary, these two manoeuvres should alsobe combined.During the last 12 years we have assessed these

reactions in over 100 cases studied clinically andpathologically and have found that full reflexhorizontal movements indicate that the lesion orlesions causing the coma lie in the cerebral hemi-spheres and not in the infratentorial brain stem. Thisrule appears to be infallible. Incomplete horizontalmovements signify a brain stem lesion which may ormay not be the sole cause of the coma. If eyemovements become impaired early in the illness,a site in the brain stem is favoured as the cause of thecoma; if impairment appears late a supratentoriallesion with a secondary effect on the brain stem(tentorial hemiation) is more likely.On this basis, it is useful clinically to divide all

coma cases into two groups, those with full reflexeye movements and those with restricted movements.It must be remembered that intoxication withbarbiturates or other hypnotics very readily paralyzesreflex eye movements, the only metabolic disorderto do so.

REFLEX EYE MOVEMENTS ON HEAD TILTING

In assessing cases of stupor and coma, we havefound that in addition to head rotation the responseof the eyes to head tilting (flexing the neck) is alsouseful, giving information about the integrity of thebrain stem from the vestibular system to the con-jugate vertical gaze centre in the region of theposterior commissure and nucleus of Darkschewitschand of the peripheral outflow of the third and fourthnerves as well. Thus the manoeuvre probes or teststhe brain stem to a slightly higher level than doeshead rotation.The test is analogous to that of head rotation:

on tilting the head forward the eyeballs are elevatedand on extending the neck the eyeballs are depressed.The excursion of the eyes is less than the correspond-ing lateral movement on head rotation. Upwardexcursion is especially limited. For better observationduring head tilting, the patient's eyelids may betaped open with adhesive rather than being heldwith the fingers.

In hemispheral lesions when full reflex horizontalmovements of the eyes are difficult to elicit, fullsymmetrical vertical excursions on head tilting maybe used as evidence that the upper brain stem isrelatively intact.

EYE CLOSURE AND ABSENCE OF BLINKING INSTUPOR

In the neurological examination of the stuporouspatient, the state of the eyelids is usually not recordedor observed. For example, closure of the lids is soobviously a part of the picture that it is apt to gounnoted. Yet it strongly suggests a parallel withnatural sleep and thereby provides a framework foranalyzing and classifying comatose states. In bothstupor and sleep, closure of the lids reflects adiminished or unsustained responsiveness to externalstimuli and probably a dearth of internal ideation.The degree of narrowing of the palpebral fissures inthe undisturbed as well as in the stimulated subjectparallels the depth of stupor and the severity ofdrowsiness. The length of time the lids remain openafter arousal is also a measure of the depth of thestupor. The onset of sleep is associated with anactive tonic contraction of the orbicularis oculi, andin stupor if the lids are only partly closed the super-imposition of full sleep results in a more completeclosing of the lids; or the slightly open eye on theside of a hemiplegia closes further. The degree oftone in the closed lid is variable and not infrequentlytrying to lift the lid evokes a brisk blepharospasm.Not always are these changes obvious on casualobservation.When a person is falling asleep, one of the first

events is cessation of blinking. Thus in theunresponsive patient if blinking persists it may beconcluded regardless of the electroencephalographicpattern that the brain stem reticular system, at leastin part, is 'awake'. Observations of blinking maytherefore be of value to the neurophysiologistinterested in signs of alertness in the 'nerve net'.Blinking varies in rate, speed of contraction andamplitude, the feeblest action being a slight medialmovement of the lower eyelid. Blinking continues inthe presence of ptosis or Bell's palsy and may occurwhen the eyelids are closed as in drowsiness.Although closing the lids and cessation of blinking

often occur together as indicators of a sleep-likestate, it is not uncommon for the lids to be closed,yet blinking continue, suggesting that lid closure is abetter index of reduced reticular activity. After anepileptic seizure the lids may be closed and thepatient almost totally unresponsive yet blinking isvery active. At other times the lids may be closedand unblinking, yet the patient, although appearingasleep, is almost awake judging from his pullingup the covers or scratching his nose or opening hiseyes when he is gently tapped or his name is quietlycalled. This state, not uncommon in large hemispherallesions, is akin to 'going to sleep' or 'being on theverge of sleep'. Other apparent dissociations between

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the depth of stupor and the state of the lids may be-seen in barbiturate intoxication where the lids maybe closed and unblinking, when a pinch on one armbrings an appropriate response from the other arm,indicating that some parts of the brain can carry onrather 'high level' activity when other parts appeardeeply asleep. In the apnoeic phase of Cheyne-Stokes respiration, the eyes may close and blinkingstop or become greatly reduced.

Usually when a stuporous patient is 'roused', theeyelids open slowly and only partially in accord withthe degree of drowsiness. There is a condition,however, in which a slight stimulus produces asudden and full, wide-awake opening of the eyes asif staring or startled. There may be little or no othersomatic reaction. Unless stimulated, the patientkeeps the eyelids closed. There is here a discrepancybetween the fully awake lid response and theappearance of sleep as judged by the lack of otherresponses and the persistent closure of the lids before-stimulation. In one of our cases it accompaniedfailure of central reflex respiration at a time whenthe limbs were still mobile and the ocular movementswere preserved to some extent.

THE 'ONE-AND-A-HALF SYNDROME-COMBINEDLATERAL GAZE PALSY AND UNILATERALINTERNUCLEAR OPHTHALMOPLEGIA

In lesions of the brain stem, vascular particularly,demyelinative or neoplastic more rarely, there-occasionally occurs a paralysis of eye movements inwhich one eye lies centrally and fails completely tomove horizontally while the other eye lies in anabducted position and cannot be adducted past themidline. Vertical eye movements are relativelypreserved. Although the explanation is straight-forward, the condition is included here because it isalmost invariably misinterpreted.

A woman, aged 79, awakened with a right hemiparesis.She was alert and gave her own history. Examinationshowed moderate weakness of the right limbs anddysarthria. The left eye did not move to the right pastthe midline. The right eye was in abduction, i.e., deviatedto the side of the hemiplegia. It could be moved towardthe left voluntarily. Two days later the patient's conditionhad deteriorated. The left eye was now fixed in the centralposition and did not move or develop nystagmus with icewater irrigation of either ear canal. The right eye movedonly from the central to the lateral position. On headrotation and ice water irrigation of the right ear canal,the right eye abducted but no other ocular motionoccurred. The patient could elevate the eyes satisfactorily.The pupils were 2 mm., equal and reactive. There wasno ptosis. At necropsy there was basilar artery thrombosiswith softening of the lower three-quarters of the left sideof the pons.

A 78-year-old woman, after complaining of headache,dizziness, vomiting, and unsteadiness on her feet for oneweek, became severely dysarthric, somnolent, andconfused. On examination she was cooperative. Speechwas slurred beyond comprehension. There was a mildright facial weakness. The tongue moved weakly. Thelimbs moved normally. The pupils were equal andreactive. There was no ptosis.The right eye was in the primary position and could

not be moved voluntarily. It abducted on head rotationand on ice water irrigation of the right ear. The left eyewas deviated outwards at rest, and voluntarily could notbe moved past the midline to the right.

We have attributed the syndrome to a lesion in ornear the pontine conjugate lateral gaze centre on oneside (causing the conjugate gaze palsy) plus aninternuclear ophthalmoplegia due to the interruptionof the ipsilateral medial longitudinal fasciculus afterit has crossed the midline from its site of origin inthe contralateral vestibular nucleus (causing failureof adduction of the ipsilateral eye). The ocularresponse on head rotation varies, depending on theintegrity of the vestibular-conjugate gaze centreconnexions.

This syndrome which we have colloquially termedthe 'one and a half syndrome' because it consists ofa conjugate lateral gaze palsy in one direction, plusone half of a gaze palsy in the other, providesevidence that the medial longitudinal fasciculus fibresrunning to the opposite ocular adductors cross tothe other side caudally in the pons near their originin the vestibular nucleus rather than runningcephalad for some distance before crossing.

DILATED, FIXED, OR HYPOREACTIVE PUPILS INTUBERCULOUS MENINGITIS

Recently our attention has been drawn to the state ofthe pupils in tuberculous meningitis.

A 17-year-old boy was admitted with a 10-day historyof headache and fever. The spinal fluid was under apressure of 410 mm. and contained 375 lymphocytes and8 polymorphs per c.mm., 153 mg. % of protein, 25 mg.%of sugar, and on smear 2 tubercle bacilli. The patient wasdrowsy. The pupils measured 7 mm., the right reactingwell, the left only slightly. The extraocular movementswere full. Six hours later the pupils were 8 mm. and fixedto light. Yet the eye movements were unimpaired. Thepatient was restless but cooperated in the examination.A left occipital burr hole was placed and during theanaesthesia the pupils narrowed to 3 mm. Next day thepatient was more alert but the pupils were still widelydilated and slow to react, particularly the left. A remark-able hippus was observed. Ophthalmological examinationshowed a fourth nerve paresis. There was no ptosis orother impairment of the muscles supplied by the thirdnerve. No clear explanation for the ocular disturbancewas forthcoming and when the patient made an excellent

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recovery on antibiotic therapy, the finding was notpursued further.More recently we were consulted concerning a woman

aged 45 with fever, headache, confusion, 190 lymphocytesin the cerebrospinal fluid, and raised intracranial pressure.In the third week of the illness the pupils were noted tohave become wider (8 mm.) and only feebly reactive tolight. The reaction on convergence was less impaired.The pupils were equal. Visual acuity was excellent. Theextraocular movements were full and there was no ptosis.The pupillary response was reminiscent of the casedescribed above and a diagnosis of tuberculous meningitiswas suggested. When therapy was changed to strepto-mycin, isoniazide, and aminosalicylate, the previouslysteady downhill course was reversed. Culture of the spinalfluid later showed M. tuberculosis. As the patientimproved, the right pupil returned to a diameter of 4 mm.and was reactive at the time when the left pupil remainedlarge and almost fixed. In a third case of tuberculousmeningitis pathologically proved, the pupils were barelyreactive at an early stage of the illness. A fourth caseshowed a remarkable hippus.

While there are no modern descriptions of thepupillary changes in tuberculous meningitis, in anolder series (Uhthoff, 1915) abnormalities werereported in 40% of cases. The pupils were unreactivein 15%, the reaction was impaired in 15%, and thepupils were unequal in another 10%. Although manyof the patients were stuporous and light perceptioncould not be adequately tested, the author felt thatlesions of the optic nerves were not the cause of thefailure of the light reaction. In addition, opticneuritis was reported in 25 %, papilloedema in 5 %,third-nerve disturbance in 18% (partial ocularpalsy eight, ptosis 10), sixth nerve paresis in 12%,-nystagmus in 10%, conjugate deviation in 8%,and other movement disorders in 1%. Hippus isapparently an uncommon event in tuberculousmeningitis and is more frequently recorded inmeningococcal meningitis.

Recognition of these ocular disturbances not onlyassists in the management of the illness but nowadayswhen tuberculous meningitis is frequently a difficultdiagnostic problem, it may even suggest the truenature of the meningitis. The mechanism by whichpupillary dilatation occurs has never been the subjectof inquiry. Exudate over the base of the brain isprobably responsible but whether the change in reac-tion is anatomically or biochemically determined canonly be speculated upon at present. The abnormalityseen in tuberculous meningitis is no doubt related toseveral other sometimes obscure pupillary changes,for example, in syphilitic meningitis, diabeticoculomotor neuropathy, and tentorial herniation.

It is appropriate here to refer briefly to theocular abnormalities seen in meningococcal menin-gitis. In one of the most thorough studies, pupillary

disturbances were recorded in 63 of 69 cases(Ballantyne, 1907).

In a recent case on our Neurology Service a youngwoman aged 21 with fever, headache, and vomiting forfour days, showed 1,200 leucocytes/c.mm. in thecerebrospinal fluid (81 % polymorphs, 19 % lymphocytes).The right pupil was 5 mm. and fixed, the left pupil 3 mm.and reactive. A striking finding was an intense injection ofthe bulbar conjunctiva of the right eye. Culture of thespinal fluid disclosed meningococci.

Ballantyne reported that conjunctival hyperaemiawas frequent, a finding not confirmed by Uhthoff.

CENTRAL PHOTOPHOBIA (CENTRAL GLARE, CENTRALDAZZLE)

This not uncommon complaint takes the form of anexcessive visual brightness, glare, or dazzle in patientswith a homonymous hemianopia. Although oftenmild, it may be the patient's main distress after anotherwise satisfactory recovery.

A patient with a massive demyelinative lesion of theright hemisphere causing hemiplegia, sensory loss,homonymous hemianopia, and apractagnosia of theminor hemisphere recovered well except for the complaint,'It's my eyes. It's the amount of light coming in, it'seither too much or too bright. I don't see clearly acrossthe room. I don't pick up details. It's not too light and it'snot too dim. The surround is affected. When it's darkerI see all right. Twilight is better. Oncoming headlights arebad. On a bright day I am dazzled as if I can't focus. Itcreates a glare and yet there is a dimness.' Examinationshowed a dense left upper quadrant-anopia and inaddition a mild left hemiparesis.Four patients with a partial left homonymous

hemianopia, presumably the result of thrombosis of theposterior cerebral artery, had a similar complaint. Onesaid that it bothered her if there was too much lightaround. Yet paradoxically she said that her vision 'justdoesn't look like daylight, it's like twilight'. The patientkept the blinds in her home drawn. Here again there wasa combination of dazzle and dimness. The second patientcomplained of the 'excessive brightness of things' whichgave him a feeling of unreality and prevented him fromfocusing sharply.The third stated that for three years after his stroke

there was an oversensitiveness to bright light. 'Thesunlight is too bright. There is so much glare from theceiling it partially blinds me.' Looking out of a windowwas unpleasant because of the brightness. He blamed thephenomenon for his poor performance on the non-verbalpart of his cortical function tests. The fourth patientnoted a 'tremendous glare' when light came from theleft, but not when it came from the right.

In the following case a visual field defect could notbe demonstrated.

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A woman, aged 69, after having had recurrent attacksof visual blurring for two weeks, suddenly developedclumsiness of the hands, dysarthria, and confusion.Immediate examination showed impaired memory andnystagmus. The signs cleared in a few days but the patientthen noted on going outdoors 'an unpleasant blurring ofvision' due to the brightness. 'I don't seem to see well.The strain is terrific. I'm living as in a nightmare.' Thesun shining on water was particularly unpleasant. Oncloudy days she could see better, and at twilight or dusk,the moon, stars, trees, silhouettes, and sharp corners ofbuildings became very plain. Neurological examinationwas normal except that on looking through a pinhole oneside seemed to be obscured, 'as if there was a threadthere'. The visual fields were full to routine testing. Thepupils were equal and reacted normally. The diagnosiswas basilar artery ischaemia with damage to the vi,ualsystem in the occipital region.

Central photophobia appears during the healingphase of the pathological process. It is probablyrelated to a lesion of the calcarine region, for it hasnot been associated with homonymous visual fielddefects resulting from infarction in the middlecerebral territory. It is probably the visual counter-part of dysaesthesias and hyperpathia arising in thedamaged somatosensory system, and of the relatedphenomena in the olfactory and other special sensorysystems.

THE LOCALIZING VALUE OF SCINTILLATIONS

In cerebrovascular disease, infarction as well ashaemorrhage, the patient may experience visualscintillations akin to those of migraine. Sometimesthese are fleeting, sometimes persistent. It is ourimpression that scintillations always indicate involve-ment of the occipital lobe, probably the calcarinevisual cortex, and never arise from involvement ofthe optic radiation as it passes through the temporallobe. They point to posterior cerebral artery diseaseand have not been observed in visual field defectsof middle cerebral origin. Since at times the posteriorcerebral artery is a branch of the internal carotidartery, scintillations may be associated with internalartery occlusion, but this is a rare event. In mostinstances the scintillations have occurred along theedges of a visual field defect.

A woman, aged 65, four days before admission whilestanding at work, lost consciousness and was foundlying on the floor. The spell lasted about five minutes.After this episode she constantly saw zigzag white lightsin the left field of vision. Many years before, the patienthad had migraine with an aura of similar zigzag lights.Neurological examination was normal. The bloodpressure was 170/130 mm. Hg. During the next monththe patient developed a left homonymous hemianopia,dysarthria, nystagnaus, cerebellar ataxia, and finally aquadriplegia. Necropsy showed thrombosis of the left

vertebral and basilar arteries with infarction of the ponsand both occipital lobes.A woman aged 58 was recuperating after myocardial

infarction when suddenly the left field of vision becamefilled with dancing lights, yellow above, white below. Atthe onset bilateral frontal headache and nausea werepresent. The initial dazzle subsided to a zigzag line oflights which outlined the medial edge of a dense leftlower homonymous quadranopia. The lights persistedwhen the eyes were closed but they were less bright. Thediagnosis was embolism to the right posterior cerebralartery.A patient, aged 56, suddenly developed a headache in

the right temple associated with flickering lights in theextreme left visual field. Examination showed a leftupper homonymous field defect. The scintillations per-sisted for five weeks. Surgical exploration revealed ahaemorrhage in the posterior extremity of the rightoccipital lobe.

THE LOCALIZING VALUE OF VERTICAL NYSTAGMUS

It is still widely held and taught that verticalnystagmus may result from upper (as well as lower)brain stem lesions. It is our experience that this iswrong. In studying the recovery of oculomotorfunction in cases of thalamic-subthalamic haemor-rhage in which paralysis or paresis of conjugatevertical gaze, both upwards and downwards, waspresent, in no case was a stage of vertical nystagmusobserved. Vertical nystagmus therefore does notreflect weakness of vertical gaze. Cases with upperbrain stemr lesions of other types were especiallyexamined for vertical nystagmus and they did notshow it. On the other hand, cases with verticalnystagmus have all had evidence of lower pontine orupper medullary mischief.

It is our conclusion, therefore, that verticalnystagmus reflects disease localized in the region ofthe ponto-medullary junction and not the upperbrain stem.

TRANSIENT DEVIATION OF ONE OR BOTH EYES

Transient conjugate deviation of the eyes associatedwith focal epilepsy and oculogyric crises is acommonplace event. Episodic deviation of one orboth eyes may occur under other circumstances,however, particularly in transient ischaemic attacksassociated with cerebrovascular disease in thevertebral-basilar territory.

(a) A man aged 59 had innumerable 30-second attacksof a giddy feeling in the head, at times associated withvertical diplopia. Twice the right side of the tongue wasnumb. In one of the spells while he was seated it was notedthat the right eye elevated to the extent of almost dis-appearing behind the upper lid and deviated slightly to the

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right. This lasted 20 seconds. Severe stenosis in thevertebral system bilaterally was shown on arteriography.

(b) A man aged 54, for three months had recurrentspells of diplopia, sweating, and dizziness lasting five to10 minutes. In one spell his wife noted that one eye wasdeviated far laterally. The patient went on to develop astroke marked by dysarthria, weakness of the tongue,left arm and left leg, and persistent nystagmus.

(c) A woman, aged 67, had brief attacks of confusion,dizziness, and diplopia. The patient's daughter observedthat in one spell upon sitting up the patient's eyes dartedfar laterally to the right side and could not be broughtback to the midline. Upon lying down the eyes returnedto the central position. In the next two weeks the patientdeveloped an extensive basilar artery infarction includinga right hemiplegia.

(d) A hypertensive man, aged 58, for four weeks hadseveral spells each day lasting five to 30 minutes,characterized by sweating, dizziness, diplopia, staggering,loss of equilibrium, occipital headache, pain in the rightnostril, icy coldness of the left side of the nose, and thewalls appeared to break into sections. His wife describedelevation of the left eye during the spell.

(e) A hypertensive man, aged 69, had six attacks lastinga few minutes of lightheadedness, blurred vision, anddeviation of the eyes to one side with inability to bringthem back to the midline position. Later spells wereassociated with diplopia, dysarthria, and weakness of theleft arm. In one attack which was witnessed, the eyesdeviated to the left and could not be brought to the rightpast the midline.

(f) A diabetic man, aged 48, in a period of one monthhad several attacks in which the right eye elevated to11 o'clock and the left eye to 1 o'clock following whichhe immediately fell 'asleep' sitting up. After five minuteshe 'awakened' and continued his scheduled activity.Hypoglycaemia was suspected, but finally in one of thespells dysarthria appeared and during the next week thepatient developed a severe brain stem infarction fromwhich he died. Necropsy showed basilar arterythrombosis.

The above cases are examples of cerebrovasculardisease with lateral or upward deviation of one orboth eyes. In the next three cases, the patients feltthat the eyes were askew.

(g) A man, aged 63, had spells three times a week ofspots before the eyes, imbalance, lightheadedness, and asensation that the eyes were crossed. 'The left eye goesover to meet the right one and seems to move aroundinterfering with vision in the right eye.' The patientlater developed a brain stem infarct.

(h) A man, aged 58, had brief attacks of numbness ofthe left face and hand, a hot feeling rising from the waist,a puff of smoke before the eyes, and a turning in of theright eye as if it were going across the bridge of the nose.

(i) Another patient, aged 75, had a single two-hour spellof diplopia in which she felt that the left eye was beingpulled out of shape toward the nose.

It is a good rule that dizziness associated with a

feeling that the eyes are 'crossing' or being pulledmedially or laterally indicates major vertebral-basilar artery ischaemia and not a more benignlabyrinthine disorder such as Meniere's syndrome.

(j) In this case, there were bouts of deviation of oneeye associated with a glioma. A man, aged 28, for 18months experienced episodes in which the left eyedeviated laterally for a few seconds without othersymptoms. Later a persistent third nerve palsy appeared.Operation disclosed a glioma involving the region of thethird nerve in the cavernous sinus region. Periodiclateral deviation of the eye had clearly preceded othersymptoms.

(k) In this case no cause for the disorder was found.The patient, aged 41, for two months had spells of verticaldiplopia lasting a few seconds up to eight hours. There wasno associated dizziness, numbness, or headache.Examination during a 30-second spell showed 50 %limitation of downward gaze in the left eye. All otherocular functions were normal.

UNWITTING CLOSURE OF ONE EYE

In this disorder the patient closes one eye withoutbeing aware that he is doing so. Not only may hedeny that he is closing the lid, he may even claimthat it is not closed. Yet on command he canreadily hold both eyes open. The patient mayerroneously be thought to have ptosis.The condition has been observed several times,

usually in brain stem disease, and it is our inter-pretation that the closure is an 'automatic' reactionof the central nervous system to the presence ofdiplopia. Although diplopia may actually be a com-plaint, or the eyes may move disconjugately, thereare cases in which the patient disclaims double vision.

A boy, 5 years of age, with increased intracranialpressure, papilloedema, and ataxia of the left leg aftera closed head injury, developed a left sixth nerve palsy.While being examined he kept the left eye closed, theright eye remaining open. This was interpreted as ptosis.However, when the right eye was covered the left eyeopened widely. When questioned in simple languageabout diplopia, the boy denied it. From our observationsit appeared that he automatically held the left eye closed.The combination of a sixth nerve palsy and isolatedptosis had posed a difficult problem.A patient, aged 64, had an intracerebral haemorrhage

associated with a right hemiparesis, dysphasia, impairedvertical eye movements, and paresis of abduction of theleft eye. When addressed, he opened the right eye butkept the left eye closed, unaware that he was doing so.On command, he kept both eyes open.A woman, aged 63, with basilar artery thrombosis, had

a 'one and a half syndrome' and in addition always keptthe left eye closed. She said she was unaware of activelyor voluntarily closing it. Yet when the right eye wascovered the left eye promptly opened.

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A woman, aged 36, with a ponto-medullary tumourcomplained of dizziness, vomiting, unsteadiness ofwalking, and 'imbalance in the eyes'. Examination showedhorizontal and vertical nystagmus and a cerebellar gait.In addition she persistently kept the left eye shut butwas unaware of this. 'My family says, "Why do yousquint out of one eye?" But I don't notice it.'A patient, aged 45, with a left hemiplegia and

anosognosia, kept the right eye squinted shut withoutrealizing it. On looking towards the left side she closedboth eyes. When asked to open her eyes she said, 'Aren'tthey open?'

It would be of no little interest if the nervoussystem should, without being aware of its action,obliterate the confusing information arising froma disconjugate position of the eyes. Almost alwaysit was the left eye that was affected.

BRAIN STEM PTOSIS

A rare event in basilar artery infarction or ischaemiais the relatively isolated finding of bilaterial ptosis.Eye movements and the pupils may be little affected.The patient remains alert. The lid droop is relativelycomplete and much greater than that of a bilateralperipheral Horner's syndrome. The mechanism of itsproduction is unknown although one might speculatethat it is the result of bilateral central sympatheticparalysis. However, the pupils have not been pinpointin our cases.

A man of 47 suddenly developed headache, dizziness,vomiting, diplopia, and both lids drooped until 'the eyeswere like slits'. Improvement occurred in six days whenexamination showed horizontal nystagmus on gaze to theleft, vertical nystagmus on gaze downwards. Theextraocular movements, including convergence, were in-tact. The right pupil was 3 mm., the left pupil 3-5 mm.and both reacted. Therewas still ptosisbilaterally, markedon the right, moderate on the left. The remainder of theneurological examination was normal. The cerebrospinalfluid contained 116 mg. % of protein. A diagnosis of brainstem ischaemia due to basilar artery thrombosis was made.In another case a 73-year-old hypertensive woman wasadmitted because of diplopia and dizziness for 12 hours.Examination showed dysarthria, left hemiparesis, rightfacial weakness, and right sixth nerve palsy. Bilateralptosis was present, the palpebral fissures being narrowedto about 5 mm. The pupils were equal and reactive.Third nerve function was intact. In a third case the patientwas subject to transient spells of dysarthria and ptosis inwhich the pupils were covered and vision was obscured.Basilar artery thrombosis occurred after three months.

ASYNCHRONOUS BLINKING

Occasionally while observing a patient it is one'simpression, usually from a sidewards glance, that

the patient does not blink the two eyelids synchron-ously i.e., one lid starts to move a fraction of asecond before the other. Our observations indicatethat this is always a sign of a very mild peripheral ornuclear seventh nerve palsy. In upper motor neuronelesions, Parkinsonism, Homer's syndrome, andptosis, blinking is synchronous. In more advanceddefects the facial weakness will be obvious.

OCULAR AGITATION (RESTLESS EYES)

Roving movements of the eyes are a common findingin many obtunded states-strokes, sleep, anaesthesia,and hepatic coma. Occasionally the movements areso brisk and exaggerated as to attract specialattention.

A woman, aged 65, suffered a right-sided stroke withaphasia three years before. Recovery was not perfectalthough speech was surprisingly good. The fingersremained weak and a brace was worn on the right leg. Onthe day of the present admission the patient graduallybecame stuporous. Examination showed an obtundedwoman whose left limbs were flaccid and immobile. Shemoved the right fingers and toes on command andmumbled a few words when addressed. The eyes wereclosed and blinking. The right limbs were spastic. Bothplantar responses were flexor. The blood pressure was200/120 mm. Hg. The cerebrospinal fluid was grosslybloody.The head was turned to the right. The pupils were

1-5 mm. and unreactive. Both eyes tended to be deviatedto the right but were subject to rapid, abrupt, violentoscillations at 75 to 100 per minute in which the eyesmoved from the left lateral position towards the centreand then darted back to the full lateral position. Therewas a slight downward motion as well. Ice-water irriga-tion of the ear canals evoked tumultuous motion of theeyes but momentarily brought them fully to the rightlateral position.

In this case the ocular agitation or restlessnessprobably had its basis in bilateral hemispherallesions, old in the left hemisphere, recent in the right.This is the most frequent cause and is illustratedfurther in the following two cases.

A man aged 86 was walking across the room when hesuddenly fell unconscious. Examination showed atrialfibrillation, deep coma, bilateral decorticate postures, andequal reactive pupils. The extraocular movements wereextraordinary in that the eyes constantly roved from oneextreme lateral position to the other, every two seconds.The patient lived two days. Pathological examinationshowed bilateral cerebral infarction. There was an oldsilent occlusion of the right internal carotid artery anda recent embolic occlusion on the left side which hadproduced bilateral infarction of the hemispheres.A woman, aged 72, in the past had had a right hemi-

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plegia and aphasia from which she recovered satisfactorily.She then developed a complete left hemiplegia andanosognosia. The eyes were deviated to the right butshowed a constant drift toward the left and nystagmoidbeating towards the right at 2 to 3 per second. The motionalso had a slight downward component.

The origin of the impulse for roving eye move-ments is at present unknown but probably lies in theupper brain stem. When hemispheral control is inabeyance bilaterally, the 'lower' mechanism appearsto operate more freely. The occurrence of spon-taenous nystagmus of this degree might be relatedto the finding that when successive hemiplegiasoccur, the eyes tend to remain deviated for a longertime after the second hemiplegia. One might haveanticipated the opposite, for if one cortical conjugategaze centre has been put out of action, the tendencyto drive the eyes to the opposite side when thesecond hemiplegia occurs should be diminished.

COMBINED WEAKNESS OF THE EXTRAOCULAR MUSCLESAND ORBICULARIS OCULI IN MYASTHENIA GRAVIS AND

PROGRESSIVE OCULAR DYSTROPHY

The selective combined weakness of the extraocularmuscles and the corresponding orbicularis oculiwith relatively preserved power in the lower facialmuscle is a distinctive sign of myasthenia gravis andof progressive ophthalmoplegic dystrophy. It is thusparticularly important in examining cases suspectedof ocular myasthenia to assess carefully the force ofeye closure and to compare it with the strength ofthe orbicularis oris. Speaking generally, weakness ofeye closure is at all times a tell-tale of facialmyasthenia.

TRANSIENT MONOCULAR BLINDNESS IN GLAUCOMA

A man, aged 63, reported that for approximately twomonths he had been having attacks of dim vision in theleft eye once or twice weekly. Everything went black for30 seconds. On the day before he came for consultation,upon arising in the morning, blurred vision had lasted forone half-hour. The patient had been struck in the righteye as a child following which he had no useful vision inthat eye although he could see vaguely in the temporalfield. Ophthalmological examination had shown thecentral retinal artery pressure to be 40 systolic, 6 diastolic.On examination, the right eye, which lay in the medial

position, had no useful vision. Visual acuity in the lefteye was 20/30. The left pupil was 4 mm. and reactedsluggishly. The fundus was normal. The extraocularmovements on the left were full. The central nervoussystem was intact. The blood pressure was 120/70mm. Hg. There were no bruits in the neck or over theeyes. The central retinal artery pressure was 70/45on the left. It could not be determined on the right. Thecommon carotid pulses were judged to be normal.

Spells of transient monocular blindness continued tooccur about three times weekly during the next threemonths. In some spells he could see only the bottom partof things, not the top. Bending over was liable to bringon an attack. One episode lasted an hour during whichvision was blurred rather than blacked out entirely. Onthe day after cyclopentolate hydrochloride (Cyclogyl)was used to dilate the pupil, the patient reported that hehad awakened with dim vision in the left eye whichpersisted until 2 p.m. On examination at 5 p.m. thepupil was still large (5 mm.). Visual acuity was 20/30.The fundus was not remarkable, and the fields were full.The central retinal artery pressure in the left eye wasextremely low. The sclera was injected, but there wasno pain.Acute glaucoma was suspected and the patient was

referred to Dr. David Donaldson. Tonometry showeda pressure of 35 mm. The angle was narrow everywhere.On Pilocarpine therapy the pressure was maintained at15 mm. for a week. While he was on this regimen thetransient attacks of blindness stopped. Narrow angleglaucoma was diagnosed and a peripheral iridectomywas carried out. There were no further episodes in thefollowing year. Two other similar cases have been studied.

OCULAR BRUIT DUE TO BASILAR-CAROTID ANASTOMOTICFLOW

A bruit heard over the eyeball originates customarilyin the internal carotid artery and is strong evidencethat the vessel is patent intracranially. There areoccasional exceptions, however, in which a distinctocular bruit is present despite bilateral occlusion ofthe internal carotid arteries.

A woman, aged 55, was lying on a sofa when thetelephone rang. She jumped up to answer it and fell tothe floor because of weak legs. She crawled to thetelephone on her hands and knees and found she wasunable to speak clearly. All symptoms cleared in 15minutes and on examination the only abnormalities weremild right facial weakness and slight dysarthria. Theblood pressure was 210/110 mm. Hg. The diastoliccentral retinal artery pressure was 16 on the right, 32 onthe left. A moderately loud systolic bruit was easilyheard over the right eyeball. The bruit persisted despitecompression of the common carotid arteries in the neckseparately and together. There were no bruits in the neck.The radial pulses were equal.

Carotid arteriography showed occlusion of bothinternal carotid arteries. On the left side, intracranialfilling occurred via the ophthalmic artery. A rightvertebral angiogram through a brachial catheter showeda large vertebral artery, the column of dye narrowing inthe basilar artery as a sign of good flow along the leftvertebral artery. The right posterior communicatingartery was 3 mm. wide and dye passed along this vesselto fill the middle cerebral and anterior cerebral arterieson both sides of the brain. The left posterior com-municating artery was small.

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In this case the bruit probably represented flowthrough the large right posterior communicatingartery. In some cases there has been an augmentationbruit in the vertebral system, i.e., a bruit resultingfrom enhanced collateral flow along the vertebralarteries in the neck. Collateral flow via theophthalmic artery from the external carotid artery,no matter how rich the supply, has never in ourexperience produced an ocular bruit.

PTOSIS ASSOCIATED WITH SUBDURAL HAEMATOMA

A man aged 75 was admitted because of dysphasia andclumsiness of the right limbs, all of uncertain develop-ment. The cerebrospinal fluid was normal and initiallya mild stroke was suspected. An unexplained finding wasa left ptosis of moderate degree, the upper half of thepupil being covered on forward gaze. A carotid arterio-gram showed a massive subdural haematoma on the leftside. This was surgically removed by Dr. Robert Ojemannand the patient recovered completely.On the day after operation the left ptosis had cleared

and did not reappear. The palpebral fissures had becomeequal. The possibility was considered that the widerpalpebral fissure on the right was the result of a rightfacial weakness and that the apparent ptosis on the leftwas actually the normal lid level. However, the palpebralfissure on the right side did not change postoperativelyand this, combined with the dramatic disappearance ofthe drooping lid favoured ptosis as the interpretation.The degree of ptosis was consonant with a Horner's

syndrome but sweating and pupillary size were notinvolved. The ptosis is tentatively attributed to amechanical effect on elements of the third nerve, althoughthere was no other evidence of involvement of the nerve.

DOLL S EYELIDS

This term designates a remarkable reflex opening ofthe eyelids when, in the comatose patient, the neckis briskly flexed. A truly doll's eyelids phenomenon!The eye-opening mechanism appears to functionfully in the presence of a 'sleeping' brain. Thereaction has been observed most often in the stuporof subarachnoid haemorrhage.

CESSATION OF BLINKING ON HOLDING THE BREATH

During auscultation over the eyeball and also duringophthalmodynamometry, excessive blinking by thepatient may pose a difficulty. It has been observedthat blinking temporarily ceases when the patient isasked to hold his breath. This simple manoeuvreshould eliminate most of the noise from the lidmusculature. At the same time the eyeballs stopmoving. It might also be mentioned here that inorder to promote relaxation of the orbicularis oculiduring these tests, having the patient let the mouthhang open loosely, will usually inhibit the tendencyto squeeze the eyes shut.

XANTHOPSIA IN DISEASE OF THE GLOBE OR OPTICNERVE

Yellow vision is a well-known accompaniment ofdigitalis poisoning. It has also been reported afterthe ingestion of santonin, trinitrophenol, and amylnitrate and in association with jaundice andeclampsia (Giesler and Wolff, 1927). It has beendescribed with sulphonamide drugs, after metrazol,and in hysteria (Walsh, 1957). We have recentlyexamined three cases in which yellow vision wasa feature.

A woman, age 36, had a subtotal thyroidectomy forhyperthyroidism. Seven months later everything beganto appear either yellow or blue. 'Things did not have anatural colour. I was colour blind.' When she read, thereappeared to be a flashlight shining in the centre of hervision. In the next seven months malignant bilateralexophthalmos with ophthalmoplegia developed and thepatient became blind in the right eye and almost so in theleft eye. Supraorbital decompression resulted in aremarkable return of vision.A man, aged 52, became blind in the right eye, over a

period of 12 hours. On the following day everything seenwith the left eye appeared yellowish and 24 hours laterthe left eye became blind. A full restoration of visualacuity took place in the next two months and a diagnosisof bilateral retrobulbar neuritis was made.A man, aged 72, on sitting up in bed at night before

going to the bathroom experienced a momentary streakof orange-yellow lightning in the left eye. It was as if thelight in the next room had been turned on and wasshining through a slightly opened door. Similar flashesthen began to appear on other occasions such as whenleaning over, turning quickly, or shaking the head.A series of three to eight streaks occurred each time. Thelight was always distinctly yellowish. A diagnosis ofMoore's lightning streaks was made.

The argument whether or not the yellow vision ofdigitalis intoxication is a peripheral or centralphenomenon remains unsettled. These three casesindicate that yellow vision at least in some instancesis a peripheral manifestation.

SUMMARY

A number of neuro-ophthalmological observationscovering 25 separate topics have been presented andbriefly discussed.

REFERENCES

Ballantyne, A. J. (1907). Ocular symptoms in cerebrospinal meningitis.Brit. med. J., 2, 190-193.

Giesler, F., and Wolff, K. (1927). Beitrag zur Xanthopsia nachDigitalis. Klin. Mbl. Augenheilk., 79, 203-208.

Uhthoff, W. (1915). Graefe-Saemisch Handbuch der Augenheilkunde,2nd ed., band 11, abt. IIA, Kap. 22, teil 2, p. 738. Engelmann,Leipzig.

Walsh, F. B. (1957). Clinical Neuro-ophthalmology, 2nd ed., Williamsand Wilkins, Baltimore.

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Some neuro-ophthalmological observations' · This paper records some neuro-ophthalmological observations made on the Stroke Service of the Massachusetts General Hospital. For the

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