The photomyoclonic reflex: artefact in the clinical … · Thephotomyoclonic reflex: anartefact in the clinical electroretinogram Fig. 1 Aphotomyoclonicreflex (PMR)wasrecorded, uncontaminatedbyretinalpotentials

British Journal ofOphthalmology, 1982, 66, 368-378

The photomyoclonic reflex: an artefact in the clinicalelectroretinogram*MARY A. JOHNSON AND ROBERT W. MASSOF

From the Wilmer Ophthalmological Institute, the Johns Hopkins University School of Medicine,Baltimore, Maryland, USA

SUMMARY An artefact may appear in the clinical electroretinogram (ERG) that can interfere withthe recording and interpretation of the ERG b wave. This artefact, the photomyoclonic reflex(PMR), was studied by covering the eye containing the recording electrode and stimulating thefellow eye. Records obtained by this technique before and after administration of a modified VanLint lid block demonstrated that most of the PMR is due to a reflex contraction of the orbicularismuscle. The remaining part of the PMR was ascertained by eye movement recordings to be a 1.5° to3 .5 downward and medial eye movement. In most persons the PMR occurs with a latency that isfast enough (59 ms+7 ms) to interfere with interpretation of the b wave under most conditions. ThePMR can be minimised in some cases by habituation or conditioned suppression. However, thesemethods generally do not extinguish the PMR but reduce it enough so that it would not readily berejected as artefact. In such cases the PMR may produce a wave form that mimics a normal-amplitude ERG but with delayed implicit time.

The electroretinogram (ERG) is a light-evoked grosselectrical potential generated by retinal cells andrecorded at the cornea. Clinically the ERG is oftenemployed to gain objective information about thestatus of the neurosensory retina.

Although much has been learned. in recent yearsabout the cellular origins of various ERG com-ponents, there still is considerable variability in theERG wave form that reflects significant contributionsto the recorded potential from extraretinal sources.For example, Gur and Zeevi,' in the course ofperforming frequency analyses on the human ERG,found that the signal is time-locked to the stimulusonly during the first 55 to 60 ms of the response. Atthat time an additional component, which was notcompletely time-locked to the stimulus, interferedwith the ERG potental. Gur and Zeevi attributed thiscomponent to a light-induced eye movement, aphotomyoclonic reflex (PMR). They citedunpublished experiments by Bickford etal.2 that were

*Presented at the 1980 Annual Meeting of the Optical Society ofAmerica in Chicago, Illinois, and at the 1981 Annual Meeting of theAssociation for Research in Vision and Ophthalnology in Sarasota,Florida.Correspondence to Dr R. W. Massof, Wilmer Institute, Rm. B-34,Johns Hopkins Hospital, Baltimore, MD 21205, USA.

said to demonstrate a reflex clonus of the eyemusculature in response to a bright flash of light.The interference from a muscular light-reflex

artefact in the recording of the ERG was first notedby Karpe.3 In his classic monograph on clinicalelectroretinography Karpe demonstrated that light-induced reflex 'blinking' can significantly impair ERGrecordability and interpretation. For example, usinga contact lens electrode and a spring-loaded speculumhe attempted to record an ERG from a retinitis pig-mentosa patient and obtained a small 'blink artefact,'in the absence of any retinal potentials, whichresembled a normal ERG except for its delayedtiming.The existence of reflexive, light-induced blinks is

well known to clinical electroretinographers. Whenthe blink artefacts are large, they are readilyrecognised in ERG records. However, less apparenteye movements that accompany all blinks4 may alsointerfere with ERG recordings.5 These eyemovements, which can occur when the lid reflex issmall or has been aborted,4 vary in amplitude andthus could be subtle enough to go clinically unnoticed.

Using the time-locking criterion of Gur and Zeevi'we have been able to identify retrospectively a PMRartefact in nearly all the records from our clinical

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The photomyoclonic reflex: an artefact in the clinical electroretinogram

Fig. 1 A photomyoclonic reflex (PMR) was recorded, uncontaminated by retinal potentials, by occluding the eye containingthe electrode and stimulating thefellow eye. (a) Control condition; no response was recorded when both eyes were covered. (b)A PMR, recordedfrom the covered experimental eye. The PMR waveform typically consists ofspikingfollowed by a fastcorneal-negative, then slow positive, phase (arrow). This reflex has a latency of55 ms. In all Figures the 10 Ps stimulus occurs atthe rising edge ofthe calibration pulse.

ERG laboratory. Furthermore we have been able torecognise this artefact in several published ERGrecords from other laboratories. Therefore thepresent study was conducted to characterise the PMRfurther and to determine its artefactual contributionsto the clinical ERG. Some of the studies reportedhere are replications of experiments that were

designed to investigate other problems or in somecases were technically unsatisfactory. Our resultsindicate that the PMR artefact can be subtle and can

significantly interfere with the interpretation of theclinical ERG.

Materials and methods

ERGs and PMRs to a full-field (Ganzfeld) stimuluswere elicited by a 10 /is white flash from a Grass PS-22variable-intensity stimulator. The luminance for a

maximal intensity (1= 16) stimulus was -0-26 log cd.s. m-2. A Burian-Allen bipolar electrode wetted withmethylcellulose was used to record the evokedresponse. The signals were amplified alternating-current coupled (0'1 Hz to 300 Hz) amplifiers. Theresponses were displayed on a storage oscilloscope,and photographed with a Tektronix C5 oscilloscopecamera.

Mydriasis was obtained with 1% tropicamide and10% phenylephrine hydrochloride. A 0-5% solutionof proparacaine hydrochloride was used in all cases as

the corneal anaesthetic.Two neutral-density filters of 1 and 2 log units

(nominal) attenuation were used in conjunction withdifferent intensity settings on the photostimulator todetermine the intensity-response characteristics ofthe PMR.

Latencies of PMRs were measured retrospectivelyfrom the records of 97 patients who had normalamplitude ERGs. Subjects for the different experi-mental manipulations included the 2 authors, 2 othernormal volunteers, and 3 volunteers who haveretinitis pigmentosa (RP). These volunteers gavetheir informed consent to the experiments.

Results

Properties ofthe PMR

Six experiments that characterise properties of thePMR are described in this section. For most experi-

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Fig. 2 Frequency distribution ofPMR latencies (mean=59ms, SD= 7 ms) measuredfrom ERG records of97 patientswith normal ERGs.

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Mary A. Johnson and Robert W. Massof

Fig. 3 The pupillary reflex is the source ofthe late positive wave ofthe PMR. (a) Arrow points to the late positive phase ofastandard-recorded PMR with normal, reactive pupils. (b) After mydriatics were instilled 2 PMRs recordedfrom the subjectlacked the late positive waves. Arrows point to areas ofthe PMR occurring at same point in time as that in (a).

ments, in order to record the PMR uncontaminatedby retinal potentials, the eye with the electrode wasoccluded and the fellow eye was stimulated.

1. QUALITATIVE FEATURES OF THE PMRThis experiment describes the PMR waveformunobstructed by the ERG.

Procedure. After 20 minutes' dark adaptation aBurian-Allen bipolar ERG electrode was inserted.The eye was then occluded by a cone covered withblack photographic tape to prevent exposure to lightduring the study. To verify the opacity of the conerecordings were obtained with both eyes occluded.The subject sat in a shielded room with his headpositioned on a chin rest facing an integrating sphere.A red light-emitting diode (LED) served as a fixationpoint for the unoccluded eye.

Results. Fig. la illustrates the results of the controlexperiment. No response was recorded when botheyes were occluded. Fig. lb illustrates the responserecorded in the occluded eye during stimulation ofthe fellow eye. The large comeal-negative deflectionhas a latency of 55 ms in this subject. The negativedeflection is usually, but not always, preceded byspiking activity, and is followed by a slower, positivewave (arrow) that has an average latency of about 160ms.The latencies of PMRs measured retrospectively

from ERG records of 97 normal patients arepresented in Fig. 2. The distribution is bell shaped;the mean is 58 9 ms and the standard deviation is 6-8ms. The range ofPMR latencies is 44-4 to 77-8 ms.

2. PUPILLARY CONTRIBUTIONS TO THE PMRThe PMR wave form becomes altered when amydriatic is instilled for ERG recording. The next

experiment is designed to assess the contribution ofthe pupillary light reflex to the PMR.

Procedure. The PMR was recorded with undilatedpupils by the procedures of the first experiment. Thecone and electrode were then removed and amydriatic was instilled into the experimental eye. Theelectrode and cone were replaced, the fellow eye wasstimulated, and responses of the experimental eyewere recorded.

Results. The long-lasting positive component of theartefact (arrow in Fig. 3a) is abolished by mydriasisof the pupil (arrows in Fig. 3b). Therefore weconclude that this late, slow potential is a pupillaryresponse to the light flash. These results and con-clusions are identical to those of Pearlman,5 based onhis studies of the ERG c wave.

3. HABITUATION OF THE PMRRepeated stimulus presentations diminished theamplitude of the PMR. The next experimentdemonstrates that the amplitude reductions are theresult of habituation rather than adaptation.

Procedure. Recordings were obtained simul-taneously from the occluded and nonoccluded eyes.Stimulus flashes were presented every 3 seconds tothe nonoccluded eye. Forty-five seconds after theflashes were terminated 2 additional flashes, 45 sapart, were presented.

Results. The ERG from the nonoccluded eyeremained constant in amplitude, i.e., no changes inadaptation occurred. Fig. 4a illustrates the responsesin the covered eye to 4 successive flashes, 3 s apart.The first response to the stimulus was the largest, thelast the smallest. Fig. 4b shows the responses to thenext 4 flashes of light. Aside from the late pupillaryresponse, the wave form is almost completely

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Fig. 4 Habituation ofthe PMR. (a). Four PMRs, 3s apart, recorded in standardfashion from one subject. Thefirstresponse is the largest negative deflection, the second response is the second largest negative deflection, etc. (b) Four responses,3 s apart, to the next 4flashes oflight show complete habituation ofthe negative wave ofthe PMR. The late positive waveis the pupillary reflex. (c) Return ofthe PMR, recorded 45 s after cessation ofhabituating stimulus. The 2 responses wererecorded 45 s apart.

abolished. Fig. 4c illustrates 2 responses, 45 s apart,recorded 45 s after the records shown in Fig. 4b. ThePMR was again elicited.The results of this experiment indicate that the

PMR becomes habituated with repeated stimulation,despite no apparent changes in retinal adaptation.This habituation presumably is under CNS control.

4. CONDITIONED SUPPRESSION OF THE PMRRecent studies have shown that the blink reflex totactile stimulation can be suppressed by auditorystimuli.67 If the PMR arises by way of a noncorticalpathway, as suggested by its short latency, it shouldnot be possible to condition it to a cross-modalstimulus, although response modification by con-ditioned suppression may be possible.

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Procedure. The PMR was recorded from theoccluded eye as described previously. A 50 ms tonewas presented, instead of the light, in order todetermine whether the PMR could be elicited solelyby the tone. The tone then was paired with the lightflash, preceding the light by 150 ms, and presentedevery 3 s for a period of IS min. After this trainingperiod the tone alone, then the flash alone, and thenthe tone followed by the flash were delivered todetermine the effects of conditioning.

Results. Fig. 5a shows that prior to conditioning thetone alone did not elicit a PMR. Fig. Sb illustratesthat the tone alone also failed to elicit a PMR afterconditioning. Thus the PMR could not be con-ditioned to the cross-modal stimulus. Fig. 5c is theresponse elicited by light alone after conditioning

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Fig. 5 Conditioned suppressionofthe PMR by an auditorystimulus. The PMR was recorded inthe standard manner. (a) Beforeconditioning, no reflex was elicitedby a 50 ms tone. (b) The tone waspaired with (presented 150 msbefore) aflash oflightfor about 15min. After this conditioning noresponse was elicited by the tonealone. A large-amplitude PMR waselicited by the light only (c), but notwhen both tone andflash werepresented (d). Presence ofthe toneahead of theflash suppressed thereflex.

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trials, and Fig. Sd is the response to the light pairedwith the tone. Figs. 5c and 5d show that, after con-ditioning, the tone suppressed the PMR, i.e., thePMR is dramatically reduced in amplitude when thelight flash is paired with the tone.These data indicate that the PMR probably has a

subcortical origin but can be suppressed by thecortex. In contrast, pupillary reflexes cannot besuppressed in this manner. Furthermore PMRhabituation and suppression rule out any putativeroles of electrotonic spread of excitation8 as thesource of the PMR.

5. CONTRIBUTION OF THE ORBICULARIS TO THEPMRKarpe3 attributed artefacts such as the PMR to dazzlereflex eyelid movements. Electroretinographers areaware that from time to time 'blinks' occur in ERGrecords. Bickford2 suggested that an eye movementrather than a blink is responsible for variations in theERG. However, in a study of blink reflexes Miles4noted that eye movements accompany all blinks,actual or aborted.

Rushworth9 measured the latencies of over 600light-induced blink reflexes in 20 patients and found amean near 60 ms. As we found for the PMR, heobserved that the blink could be elicited in thecontralateral eye, that it could show habituation, andthat it did not become conditioned to an auditorystimulus. The next experiment was designed todetermine the contribution of a blink to the PMR.

Procedure. A modified Van Lint lid block wasperformed on one of the authors with 10 ml of a 50:50mixture of 2% lignocaine and 075% bupivacaine,with added hyaluronic acid. The subcutaneous tissueswere infiltrated with the anaesthetic solutionsurrounding the orbital rim and extending back 4 cmtoward the tragus of the ear. This lid block wasclinically complete in paralysing the orbicularismuscle within 15 min, resulting in the subject'sinability to close the eye, and lasting for about 3hours.

Prior to the lid block ERG electrodes were placedin both the occluded and nonoccluded eyes, and theERG and PMR were simultaneously recorded. thisprocedure was repeated after the orbicularis of theoccluded eye was completely paralysed by the lidblock.

Results. Fig. 6a shows that the PMR was present inboth eyes prior to the lid block. The top trace is thePMR superimposed on the ERG from the unoccludedeye. The bottom trace is the PMR from the occluded,experimental eye. Note that the PMR is consensual.

Fig. 6b illustrates the PMR after the orbicularismuscle of the occluded eye is paralysed. As before,the PMR was elicited in the nonoccluded eye (top

trace). As seen in the bottom trace, paralysis of theorbicularis eliminates the spiking and the initialnegative potential of the PMR. However, a smallcorneal-positive potential remains.These data indicate that the major portion of the

initial corneal-negative wave form of the PMR can beattributed to contraction of the orbicularis.

Fig. 6 Role oforbicularis muscle contraction in the PMR.Electrodes were placed on both eyes, and one eye wasoccludedfrom the light. (a) The top traceshows the ERG andPMR recordedfrom one eye, and the bottom traceshows justthe PMR recordedfrom the occluded fellow eye. (b) Amodified unilateral Van Lint lid block was then administeredto the covered eye. Twenty minutes later the light-elicitedresponses were again recordedfrom both eyes under thesameconditions. Most of the PMR was eliminated by the lid block(lower trace), indicating substantial contributionsfrom theorbicularis muscle.

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Fig. 7 Double-exposurephotograph showing small eye andeyelid movements. Photograph wastaken in a dark room with thecamera shutter held open. The lightsource was a strobe, triggered todoubleflash with an interflashinterval of 120 ms. Note the 2displaced corneal reflectionsfromthe strobe and the displaced imagesofthe scleral vasculature andeyelashes.

Furthermore, because the initial spiking waseliminated, we conclude that it too may be attributedto the orbicularis. This latter conclusion is inagreement with Kennard and Glaser,'° whoattributed spiking in blink reflex records to nervousinnervation of the orbicularis muscle.

6. THE ROLE OF EYE MOVEMENTS IN THE PMRThe residual response in Fig. 6b may be due to a smalleye movement. This hypothesis is consistent with thefinding by Miles4 that all blinks, whether actual oraborted, are accompanied by eye movements. Thefollowing experiments examined this possibility.

Procedure. We recorded reflex movement of theeye by photographing the eye before and during thePMR. In a dark room a camera was focused on thesubject's eye, and the shutter was opened. A doublestrobe flash was then delivered to the subject. Theinterval between flashes was 120 ms, which is roughlythe implicit time of the PMR.An accurate determination of the amplitude and

direction of this eye movement was established by thefollowing procedure. A Burian-Allen bipolar ERGelectrode was placed on one eye to record thepresence of the PMR. The other eye contained ascleral eye coil which, when the subject was placed ina magnetic field, could record eye movements with aresolution of less than 30 minutes of arc (for methods,see Robinson" and Collewijn et al. 12). A strobe flashwas used as the stimulus.

Results. The double-exposed photographs showedsmall movements of the eyelid and eye in the 3subjects tested. Fig. 7 is a typical photograph fromone subject. Note the 2 displaced comeal reflectionsfrom the strobe, and also displaced images of the

scleral vasculature and the eyelashes. Thisobservation supports the hypothesis that the remnantof reflex after the lid block can be attributed to eyemovement.

Data from the scleral coil eye movement recordingsare shown in Fig. 8. Figs. 8a and b are records obtainedduring the same light flash. Fig. 8a is the record fromthe ERG electrode, which shows that aPMR having alatency of 55 ms (arrow) occurred in response to thelight flash. Record 8b from the eye coil shows an eyemovement with a latency of 65 ms, occurringdownwards and medially. Eye movements from the 2subjects tested had amplitudes ranging from 1-5° to3.50These data show that eye movements occur in con-

junction with reflex blinks during a PMR. The eyemovements have slightly longer latencies andapparently produce smaller potentials than eyelidmovements.

Clinical ERG Interpretations and the PMR

Important considerations for assessing the impact ofthe PMR on ERG interpretation must include: (1)the timing of the PMR in relation to the variouscomponents of the ERG, and (2) the shape of thePMR wave form and how it may distort or mimic theERG wave form. These aspects of the PMR areexplored in the next set of experiments. Also, a briefstudy comparing the propensity of several popularERG electrode types to record the PMR is described.

7. INTENSITY-RESPONSE CHARACTERISTICS OFTHE PMRWe obtained an intensity-response function for the

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Fig. 8 Extent ofeye movements in a PMR elicited by a strobeflash were measured by a scleral eye coil. 2 (a) Recordfrom astandard ERG electrode which was placed on thefellow eye to record the presence ofthe PMR. The arrow points to PMRonset. (b) Eye movement recordings. Calibrations were obtained by saccadic pursuit ofstepwise horizontal or verticaldisplacements ofafixation spot. Horizontaland vertical components ofthe light-elicited reflex eye movement were recorded on2 separate channels ofa pen writer. The horizontal component (up=rightward movement) ofthe eye movement measured inthe subject's right eye has a latency ofabout65 ms and an average amplitude ofabout3° in this subject. The vertical component(up=upward movement) occurs simultaneously with the horizontal component and has an average amplitude ofabout 2" inthis subject. Consequently the direction ofthe eye movement was toward 7o'clock (downwards and medial) with an amplitudeofabout3 5°.

PMR in order to determine how the latency andamplitude related to stimulus strength.

Procedure. The PMR was recorded from theoccluded eye by the procedures described above.Stimuli of increasing intensity, covering a range of 3log units, were presented to the unoccluded eye.Results were compared with ERG records obtainedat an earlier date from the same subject by means ofthe same stimuli and order of stimulus presentation.

Results. We found that the amplitude of the PMRdoes not depend on stimulus strength in any pre-dictable fashion; amplitude depends mainly on thestate of habituation. However, there is a PMRthreshold, which varied between observers. Latencyon the other hand decreased slightly (from 67 to 56ms) over a 3 log-unit increase of intensity (Fig. 9). Todetermine the effect of PMR latency change (or lackof it) on ERG interpretation, the implicit times (timefrom stimulus onset to peak of the wavelet) of ERG bwaves, obtained under the same stimulus conditionsas the PMR, were plotted along with the PMR data.(The b wave implicit time was selected for comparisonbecause the appearance of the b wave in patientsusually forms the basis forERG evaluation.) As seenin Fig. 9, the graphs of the 2 functions cross at 57 ms.For example, for this subject at all but the 2 highestintensities the PMR starts at a time before the b wavereaches its peak amplitude.The effect of PMR on ERGs elicited by a low-

intensity (-2-16 log cd. s. m-2) and a high-intensity

(-026 log cd. s. m-2) stimulus is shown in Figs. 10,11, and 12. Fig. 10 shows a maximal-amplitude ERG(a) and an ERG elicited with about 2 log units less

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LOG INTENSITY (cd-sec m2 )Fig. 9 Latency ofthe PMR and b wave implicit time as afunction of intensity in log cd. sec. m-2. Over a 3-log unitrange of intensities the b wave implicit time markedlydecreased, while the PMR latency showed only a slightreduction. The graphs ofthe 2 functions cross atapproximately -O-7 log cd. s. m-2 (57ms), indicating thatformostofthe dynamic range ofthe b wave, the PMR willoccurbefore the b wave peak.

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Fig. 10 The effect of the PMR on normal ERGs. (a) TwoERGs elicited by a stimulus intensity (-026 log cd. s. m-2)that produces a maximum amplitude ERG. (b) Two ERGselicited by a stimulus intensity (-2-16 log cd. s. m-2) thatproduces about a half-maximum amplitude ERG. The reflexcompletely obscures interpretation of these ERGs because ofthe different intensity-response characteristics of the ERGand PMR. The PMR would not become habituated in thissubject.

intensity (b) from a normal volunteer. In this case thereflex occurs slightly faster than for the subjectreported above (Fig. 9), making measurement of theamplitude of the maximal-amplitude ERG difficult,and measurement of the amplitude of the lower-amplitude ERG impossible (because the implicit timeof the b wave increases as the stimulus intensitydecreases).

Fig. lla illustrates ERGs from another subject inresponse to a light intensity that evoked a maximalamplitude ERG. Repeated, predictable deliveries ofthe stimulus habituated the reflex and eventuallyproduced a totally time-locked b wave response

(Figs. 1 lb and c). Fig. 12a illustrates 2 ERGs from thesame subject, elicited by light of about 2 log units lessintensity than that in Fig. 11. Note how the apparentimplicit times of the b waves changes with habituationof the PMR. Fig. 12b is a record of 10 consecutiveresponses to the same conditions after habituation ofthe reflex was achieved.

8. POLARITY OF THE PMRWe noticed in some cases that the polarity of theinitial negative deflection of the PMR was reversed.The polarity of the pupillary response, however,remained corneal-positive in these individuals. PMRsof inverted polarity closely resembled ERGs ofnormal amplitude and delayed timing. The polaritychange could be attributed to electrode position inrelation to the standing field potential of the eye. Ifthe initial position of the electrode was at the mostpositive pole of the eye, then any movements of theelectrode or the eye would be expected to produce anegative deflection. In contrast, if the electrode'sinitial position was away from the most positive pole,then movements bringing the electrode positioncloser to the pole would be expected to produce apositive response. To test these possibilities the effectof initial ERG electrode position on the polarity ofthe response of voluntary eye movements wasdetermined in the next experiment.

Procedure. The relative position of the electrodewas changed by instructing the subject either to fixatea red LED directly in front of him, allowing theexaminer to obtain central positioning of the contactlens on the cornea, or to fixate about 15° above orbelow the LED, with his head still orientated directlyforwards, allowing the examiner to obtain eccentricpositioning of the contact lens in relation to the centreof the cornea. The subject was then instructed toexecute a voluntary eye movement-either up,down, left, or right-when cued by a flash of light.

Results. A corneal-negative potential was recordedwhen the 2 subjects, fixating centrally, looked up. Asimilar potential was recorded when the subjectdirected his fixation from centre, either downwardsor to the left or right. The potential was corneal-positive when the subject fixated eccentrically andmoved his gaze to the centrally located LED. Thus,depending on the position of the contact lens inrelation to the center of the cornea, normal eye blinksand movements of the eye under the electrode duringERG recording could result in either corneal-positiveor corneal-negative PMRs.

Small corneal-positive PMRs, regardless of theirorigin, which occur in patients who have extinguishedor severely reduced ERGs can easily be misinter-preted as being ERGs, because, as Karpe demon-strated, these PMRs can closely resemble retinal

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Fig. I1 The effect ofhabituationon the maximal amplitude ERG.(a) Two ERGs recordedfrom a

normal subject. Note how the ERGwaveform breaks down at the peakofthe b wave where the PMRbegins. (b) Recorded duringhabituation, these 4 ERGs begin toshow less variation in waveform.(c) The next 4 ERGs recorded arevirtually superimposable because ofthe nearly total habituation ofthePMR.

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potentials. The epitome of this imitation is the clinicalERG shown in Fig. 13a, recorded from a patient withretinitis pigmentosa (RP). Because the responsewould not become habituated, it was not until the eyewith the electrode was occluded and the fellow eyewas stimulated (Fig. 13b) that the identity of thepotential as a PMR was conclusively established.Note how closely this PMR resembles an ERG ofnormal amplitude but delayed timing.

Distortion of the ERG by the PMR has beenobserved similarly with various other patients. Forexample, the top trace of Fig. 14 shows the ERG

record obtained from another RP patient. The larger,slower potential could be interpreted as a delayed rodb wave, thus giving rise to abnormal splitting of rodand cone components. However, in this case habitu-ation eliminated the PMR contribution to thepotential, and the patient's actual ERG is shown inthe middle trace of Fig. 14.

9. EFFECT OF ELECTRODE TYPE ON THE

RECORDABILITY OF THE PMR

Several different types of electrodes are at presentused to record the clinical ERG. We tested 3 of the

Fig. 12 Theeffectofhabituation on ahalf-maximum amplitude ERG. (a) Two ERGs recordedfrom a normalsubjectusingthe lower-intensity (-2 16 og. cd. s. m-2) stimulus. Note that the apparent implicit times ofthe b wave change with habituationofthe PMR. (b) Ten consecutive ERGs, recorded 3 s apart, after habituation ofthe PMR. The waveform is now totallytime-locked to the stimulus.

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Fig. 13 The PMR in retinitis pigmentosa (RP). (a) This record was obtained during ERG testing ofan RP patient. Thewaveform resembles a normal amplitude ERG delayed in implicit time. (b) The eye containing the electrode was occluded, andthe fellow eye was stimulated. Records obtained in this manner show that the waveform is artefactual.

most popular electrodes-the Burian-Allen bipolarelectrode, the Burian-Allen monopolar electrode,and the gold foil electrode-comparing their sensi-tivity to recording the PMR.

Procedure. Because the Burian-Allen bipolarelectrode was used throughout this study it became a

reference in this experiment, recording the PMR inone eye while the gold foil or monopolar electroderecorded the PMR simultaneously in the occludedfellow eye. This manipulation permitted us todetermine when the PMR was present and also toevaluate its recordability after habituation. Thecontrol experiments were performed, in which both

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Results. The monopolar electrode recorded a loweramplitude PMR than was recorded by the bipolarelectrode. This reduction in amplitude of the PMRappears to be mainly due to a reduction in record-ability of the lid component; no extremely largePMRs were noted, and onset spiking was absent frommost records. The main difference between the 2electrodes is that the indifferent electrode is locatedin the speculum of the bipolar electrode, whereas it isplaced on the patient's forehead for the monopolarelectrode. Although the amplitude of the PMR

Fig. 14 ThePMRinRP. The toptrace shows 2 ERG traces obtainedfrom an RPpatient duringstandardERG testing. The larger, slowerpotential could be interpreted as a

delayed rod b wave, thus giving riseto abnormal splitting ofrod andcone components. Habituation inthis case eliminated the PMR andrevealed the patient's actual ERG

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recorded by the monopolar electrode was reduced,the response often closely resembled a delayed ERG.The gold foil electrode was very sensitive to

recording the PMR, possibly because it touches thelower lid, and a strong medial movement of the lowerlid occurs during actual or aborted blinks. ' The sizeof the PMR relative to that recorded with the bipolarelectrode was quite variable during different sessions.This variability probably can be attributed to variableplacement of the gold foil electrode and repositioningof the electrode by blinks.Very little habituation was observed during testing

of either the monopolar or gold foil electrode, despitehabituation observed in the fellow eye with thebipolar electrode. In the case of the monopolarelectrode lack of habituation may be due to the factthat the PMR recorded by this electrode was alreadyquite small and may have mainly been due to thereflex eye movement. It is possible that the blink wasbecoming habituated, but the eye movement was not.In the case of the gold foil electrode even minormovements of the lower lid may have produced asufficiently large response as to obscure signs ofhabituation.

In contrast it appears that the PMR cannot berecorded with the Henkes electrode. Van Norren(personal communication) indicated that hereplicated the main experiments described here usingthe Henkes electrode, and when the experimentaleye was occluded and the fellow eye stimulated noPMR could be recorded. Van Norren's failure torecord the PMR probably can be attributed to the factthat the Henkes electrode is held on the cornea by anegative pressure; consequently the electrode moveswith the eye and probably is not displaced by blinks.

Discussion

The present study has confirmed and described morefully an artefact that exists in the clinically recordedERG. This artefact is a photomyoclonic reflex,consisting largely of eye lid movements and to a lesserextent eye movements. The mean latency of thePMRis approximately 59 ms.

It is important to recognise the appearance of thePMR in ERG records, because it can interfere withthe recording and interpretation of both theamplitude and the latency of the ERG. The eyelidmovement reflex can be habituated by regular,repeated, predictable stimulus presentations in somebut not all subjects, and habituation, when it occurs,may occur to a different extent among varioussubjects. The eye movement contribution to the

reflex does not appear to become habituated aseasily, and may thus subtly affect interpretation oflow-amplitude or nonrecordable ERGs. Partiallyhabituated lid movements may also insidiouslyinterfere with ERG interpretation, especially if thepolarity of the potential is corneal-positive.

Burian-Allen bipolar and gold foil electrodes aremore susceptible to recording the artefact, the formerbecause of the placement of the indifferent electrodein the speculum, the latter because it rests on thelower lid, which moves medially with every actual orattempted blink.'Because recording the PMR may be unavoidable

with most electrodes, it is important to recognise thisspurious wave form in ERG records. Often, but notalways, identification of the PMR when using abipolar electrode is facilitated by observation ofspiking activity at the onset of the reflex.

This work was supported by research and core facility grants EY-01791 and EY-01765 from the National Eye Institute, and by aResearch Center grant from the National Retinitis PigmentosaFoundation.

We thank F. W. Fitzke, D. Guyton, A. Lasker, C. Perry, and D.Robinson for technical advice and assistance, D. Andrews and D.Finkelstein for comments on the manuscript, G. Fishman of theUniversity of Illinois Eye and Ear Infirmary for the loan of themonopolar electrode, and D. van Norren of the Institute forPerception in Soesterberg, the Netherlands, for permitting us to citehis unpublished study.

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The photomyoclonic reflex: artefact in the clinical … · Thephotomyoclonic reflex: anartefact in the clinical electroretinogram Fig. 1 Aphotomyoclonicreflex (PMR)wasrecorded, uncontaminatedbyretinalpotentials