British Journal ofOphthalmology, 1982, 66, 382-385

Visual evoked response in transientmonocular visual lossLANNING B. KLINE' AND JOEL S. GLASER2

From the 'Eye Foundation Hospital, Department ofOphthalmology, University ofAlabama, Birmingham,Alabama, and the 2Bascom Palmer Eye Institute, Department of Ophthalmology, University ofMiami, Miami,Florida, USA

SUMMARY The pattern-reversal visual evoked response (VER) was recorded in 2 patients duringtransient monocular visual reduction. In both cases the VER was initially abolished. With recoveryof vision there was gradual return of amplitude over a 3- to 8-minute period, while latenciesremained unchanged from preattack values. These findings are discussed with regard to currentunderstanding of the origins of the VER and relevant aspects of retinal electrophysiology.

Amaurosis fugax typically is the result ofretinal micro-embolisation, classically from occlusive disease of theextracranial carotid artery,' or from other sources.2-6Rarely, retinal vasospasm has been documented as acause of transient visual loss. "-' We had the oppor-tunity to record the visual evoked response (VER)during monocular loss and subsequent return ofvisionin 2 patients. While other aspects of these cases weredescribed elsewhere,89 the unique opportunity torecord the VER prompted this report. To the best ofour knowledge the VER has not been previouslyrecorded during transient monocularvisual reduction.

Materials and methods

During attacks of transient monocular visual loss theVER was obtained in different laboratories. Never-theless the basic technique was similar, employingpattern-reversal stimulation with large checks (60' to80' of arc) at low frequency (1-3 Hz), recording tran-sient responses in each case.Our first patient, wearing appropriate refractive

error, was positioned 75 cm in front of a screen on towhich was projected a high-contrast black-and-whitecheckerboard pattern. The entire pattern subtended230 of central visual field with each individual squaresubtending 60' of arc. The average luminance at thescreen was 270 cd/M2. Reversal was produced byangular oscillation (1-2 Hz) of a mirror. Occipital

Correspondence to Dr Lanning B. Kline, Eye Foundation Hospital,1720 University Boulevard, Birmingham, Alabama 35233, USA.

potentials were recorded with bipolar disc electrodesplaced in the midline located 1 cm above the inion andat the vertex; an indifferent electrode was attached tothe ear. The signal was passed through a preamplifier(Grass P-15) and a differential amplifier (Tektronix3A9). Between 64 and 128 responses were averaged(Nicolet 1072 computer-averager) in at least 2 sep-arate runs for each measurement. An observermonitored patient fixation throughout the courseof VER testing. This technique produced a VERcharacterised by a small upward and larger downwarddeflection at approximately 100 ms. The negativecomponent had the largest amplitude and was themost reliable complex. Latency was measured fromthe onset of the stimulus to the peak of this majornegative component.VER recordings for the second patient were ob-

tained with a monopolar lead 1 cm above the inionand with a reference electrode at the mastoid process.The wave forms were recorded with a Nicolet CA-1000 system with television pattern generator. High-contrast black-and-white alternating check stimuliwere presented at a reversal rate of 3 Hz, and 128transient responses were averaged. At a distance of 4feet (120 cm) each check subtended 80' of arc, withthe entire screen subtending 100 42' horizontally and8° 30' vertically. Patient fixation was monitored con-tinuously by an observer. With this technique theVER was characterised by a small negative deflectionand larger positive component at approximately100 ms. Latency was measured from the onset of thestimulus to the peak of this major upward deflection.

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Visual evoked response in transient monocular visual loss

Fig. I Case 1. Fluoresceinangiography ofrightfundus, 55seconds after onset ofamauroticfugax, demonstrates dye withinvessels ofthe optic disc andsegmental, incompletefilling ofjuxtapapillary retinal arterioles andveins. (Reprintedfrom Shawet al.8).

unchanged, measuring 94 ms (normal: 98±16 ins).Case reports and results

CASE 1A 23-year-old black woman had recurrent amaurosisfugax in her right eye for 3 months. When she wasinitially examined, her visual acuity was 20/20 in eacheye. Visual field examination showed a superiorarcuate scotoma in the left eye. Ophthalmoscopy re-vealed dilated arterioles and veins in the right eye.The left fundus showed areas of vascular sheathingsuggestive of previous vasculitis. The remainder ofthe examination was normal.

During examination the patient had repeatedamaurotic attacks in the right eye. Right vision wasinstantaneously reduced to no light perception, with anonreactive, amaurotic right pupil. Ophthalmoscopyrevealed narrowing of retinal arterioles and veins,cessation of retinal blood flow, segmentation of theblood columns, and optic disc pallor. During anepisode of transient visual loss fluorescein angio-graphy showed early filling of the right optic disc andperipapillary capillaries, but fluorescein dye was notseen in the retinal arterioles until 30 seconds afterinjection (Fig. 1). The patient was found to haveboth SC haemoglobinopathy and systemic lupuserythematosus. After treatment with prednisone theamaurotic attacks abruptly subsided. The patient hasremained asymptomatic.VER was obtained at the onset of amaurosis fugax,

and after 2, 5, 8, and 11 minutes (Fig. 2). At the onsetof the attack no VER was recordable,and with returnof retinal perfusion the VER amplitude graduallyincreased over a 5-8-minute period. In contrast,as VER amplitudes returned, latencies were

CASE 2Four days prior to examination a 48-year-old manreported the onset of repeated episodes of 'almost

PRE-ATTACK ;f\

ONSET OF ATTACK

2 MIN. AFTER ONSET

5MIN. AFTER ONSET

8 MIN. AFTER ONSET

I I MIN AFTER ONSET

15juvSOrmec

V

.-

I

Fig. 2 Case 1. Serial recordings ofpattern-reversal VERduring an attack ofamaurosisfugax on the rightdue to spasmofthe central retinal artery.

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Lanning B. Kline and Joel S. Glaser

Fig. 3 Case 2. Fluoresceinangiography ofthe left eye 8seconds after the onset ofocularmigraine revealsfilling of retinalvessels only inferotemporally. Theremainder ofthe vessels filledapproximately 30 seconds later.(Reprintedfrom Kline and Kelly9).

total blindness' of the left eye lasting about 2 minutes.During these episodes he experienced progressiveloss of peripheral visual field but maintained a smallportion of central visual field, which he described as

'shaped like a leaf.' The patient had experiencedclassic cluster headaches for the past 25 years butnone in the previous 6 months. There was no familyhistory of migraine. While he was asymptomatic,

PRE - ATTACK

ONSET OF ATTACK

1 MIN. AFTER ONSET

2 MIN. AFTER ONSET

3 MIN. AFTER ONSET

A5gv

50 msec

Fig. 4 Case 2. Serial recordings ofpattern-reversal VERduring an episode oftransient visual reduction ofthe left eyedue to ocular migraine.

neuro-ophthalmological testing was entirely normal,including funduscopic examination.While he was in hospital the monocular attacks

of visual reduction, each lasting approximately 2minutes, were studied in detail. The patient main-tained visual acuity of 20/30 on the left, and a smallcentral island of visual field. During the attacks theretinal veins narrowed. There was delay in theappearance of fluorescein dye in branches of thecentral retinal artery yet prompt filling of 2 cilioretinalvessels (Fig. 3). Haematological and cardiac investi-gations, including echocardiography, gave normalresults, and no abnormalities were found on carotidangiography. Diagnosed as having ocular migraine,the patient was placed on propranolol, with promptcessation of visual symptoms.As seen in Fig. 4, at the onset of the attack of ocular

migraine the VER was abolished. While amplitudereturned over a 2-3-minute period, the latencies(102 ms) were essentially unchanged from preattackvalues (normal: 99 ms+7).

Discussion

The series of electrical and electrochemical eventsthat leads to the elaboration of the VER begins in thephotoreceptors of the retina and culiminates in theoccipital cortex. Pattern-reversal VER has beenfound to show a more consistent waveform and to bemore sensitive in detecting lesions of the visual path-ways than has flash response. ' In the assessment ofafferent input to the visual cortex pattern-reversalVER has been studied in a variety of diseases of theoptic nerve, including optic neuritis, " ischaemic optic

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Visual evoked response in transient monocular visual loss

neuropathy, 2 13 toxic amblyopia, 4 glaucoma,'" andcompressive optic neuropathy. 6 Comparison ofamplitude and latency abnormalities has at times dis-tinguished among such optic nerve diseases. Forexample, in the acute phase of demyelinative opticneuritis the amplitude of the pattern-reversal VER isreduced, and it returns to normal with clinical re-covery, while characteristically prolonged latencyremains. " However, in many instances it is difficult toseparate the relative contribution of axonal degenera-tion and demyelination when VER abnormalitiesoccur.The 2 cases presented here provide an opportunity

to examine selective impairment of axonal trans-mission within the optic nerve without disturbance ofmyelin sheaths. The central retinal artery is the solevascular supply of the inner retinal layers (ganglioncells, inner plexiform layer, inner nuclear layer)."With temporary interruption of blood flow, innerretinal activity ceases and no VER is generated. Withresumption of blood flow there is progressive in-creases in retinal neuronal function, and VER ampli-tude gradually returns (Figs. 2 and 4). But withgradual return of inner retinal function there is never-theless a constant value for VER latency.

Investigations into the genesis of the VER havedealt with contributions from striate (area 17) andextrastriate (areas 18 and 19) cortex.'820 An under-standing of the relationship between the VER andunderlying neural events is far from complete. Theonly study dealing with the origin of the transientpattern reversal VER was done by Halliday andMichael,'8 who found that the largest amplitude res-ponses were recorded at electrodes located 5 to7-5 cm in front of the inion, a site anterior to thestriate cortex. They concluded that the major deflec-tion occurring at approximately 100 ms is generated inextrastriate cortex.Our studies demonstrate that return of inner retinal

function, with no damage to optic nerve myelin,causes no alteration in VER latency. This phenom-enon suggests that the inner retina responds in anall-or-none fashion. Current understanding of retinalelectrophysiology supports this interpretation. Withvisual excitation the majority of retinal neural cellsrespond in a slowly graded manner, with the excep-tion of retinal ganglion cells and some amacrine cells,where depolarisation leads to an all-or-none actionpotential.2'22 With interruption and subsequent re-turn of inner retinal activity there is a gradual andprogressive return of VER amplitude, presumably

reflecting the number of functioning ganglion cells.yet an immediate restitution of latency occurs, pos-sibly due to the all-or-none action potentials of theretinal ganglion cells.

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