suprathreshold vision in acute optic neuritis

Journal of Neurology, Neurosurgery, and Psychiatry 1982;45:227-234

Suprathreshold vision in acute optic neuritisJ SJOSTRAND, M ABRAHAMSSON

From the Department of Ophthalmology, University of Goteborg, Gdteborg, Swedeni

SUMMARY The perception of contrast was measured in patients with acute unilateral optic neuritisby a technique of subjective suprathreshold contrast matching, and was compared with contrastsensitivity as defined by threshold measurements. The suprathreshold apparent contrast andthreshold contrast sensitivity was repeatedly assessed during the recovery phase. Generally, anattenuation of suprathreshold apparent contrast was found for high and intermediate spatialfrequencies in the eye with optic neuritis. At a low spatial frequency, however, the suprathresholdcontrast vision was spared. The threshold contrast sensitivity was not however, spared at lowspatial frequencies. During recovery this frequency-specific loss in suprathreshold apparent contrastdiminished and finally a "normal" suprathreshold contrast vision was observed in all affected eyesreaching a visual acuity of 1 0 or better. In these cases also subjectively normal vision was reportedin spite of a persisting abnormality in threshold contrast sensitivity.

Over the past two decades the use of spatiallyperiodic stimuli has increased our understanding ofvisual processes in the normal human visual system.12During the last decade visual stimuli in the form ofsinusoidal gratings have been increasingly used as atest of the contrast processing of the normal anddiseased visual system.3 In ophthalmological diseasesaffecting the ocular media or the retina, the contrastthreshold for sinusoidal gratings of different spatialfrequencies has been found to be abnormal.4-7Contrast sensitivity, defined as reciprocal of thres-hold contrast also has been shown to be impaired indiseases of the retrobulbar optic pathway.8-12

In a previous study of acute optic neuritis ageneralised impairment of the contrast sensitivityfor all spatial frequencies was found.9 This findingwould imply that the detectability expressed as theminimum contrast necessary to detect the presenceof a stimulus pattern of all angular sizes is impaired.However, patients with optic neuritis often complainthat objects in the visual scenery with high contrastare also dimmer and lose contrast. This perceptionabnormality experienced by patients with opticneuritis indicates a disturbance in suprathresholdvision. Investigations of the suprathreshold contrastvision of normal subjects have demonstrated that

Address for reprint requests: Dr Johan Sjostrand, Departmentof Ophthalmology, Sahlgren's Hospital, 413 45 Goteborg,Sweden.Received 8 February 1981 and in revised form 25 September1981. Accepted 3 October 1981

characteristics of the threshold contrast sensitivitycannot be extrapolated to suprathreshold levels.13 14Suprathreshold matching experiments in normalobservers show that contrast sensation becomesindependent of spatial frequency at higher contrastsunlike the case at threshold contrast. Our know-ledge, however, of the contrast vision above thres-hold in disease is extremely limited.13 15

In daily life mainly suprathreshold contrast visionis used for pattern recognition and the aim of thepresent study was therefore to study suprathresholdapparent contrast during the acute phase and recoveryof optic neuritis, a disease that produces a profoundand longlasting impairment of threshold contrastsensitivity.9 12 In the acute phase of optic neuritisthe contrast sensitivity is depressed for all spatialfrequencies but during resolution of the disease thesensitivity partially recovers.9 This study wasdesigned to investigate the changes of contrastperception above threshold during the recovery phasein patients with acute unilateral optic neuritis.During the acute phase the suprathreshold contrastmatching was abnormal but during resolution anormalisation occurred owing to some suprathres-hold compensation of persisting threshold contrastsensitivity deficits.

Patients and methods

Patients Eight normal controls (age 25-47 years) andfive patients with acute optic neuritis (age 22-66 years)took part in this study (table). Every patient was sub-

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Sjostrand, Abrahamsson

jected to a careful neuro-ophthalmological examination.Three patients had isolated unilateral, retrobulbar opticneuritis of presumably demyelinating nature; thediagnosis was based on the criteria defined by Gouldet al.16 Two cases had multifocal symptoms and signs ofneurological dysfunction indicating the diagnosis ofmultiple sclerosis. In all cases acute symptoms of blurredvision occurred in only one eye. At each visit the subjectswere examined opthalmologically and the visual acuitywas determined. Monocular visual acuity was determinedwith best correction at a test distance of 5 m using thenatural pupil. An officially approved acuity chart(KIFA: Monoyer-Granstrom) illuminated with approxi-mately 700 cd/M2 in a LIC universal light box was used.Visual acuity of the eyes with optic neuritis ranged from0-1 to 1-0 and the acuity in the contralateral eyes were1-0 or better.

The task of the patient was to adjust with a continuousattenuator the contrast of the variable grating until itmatched the photographic, non-variable one inapparent contrast. Fifteen different photographic gratingswere presented twice during the test at the spatial fre-quencies (0 7, 2-7, 6-2 cycles/degree) and at five contrastlevels (0-85, 0-60, 040, 0-25, 0-15) for each frequency(fig 1). Owing to small variations in the photographicalprocedure small differences in contrast levels of thephotographic gratings occurred at different frequencies.The actual contrast values were 0 85, 0-57, 0-42, 0-31,0-18 and 0-85, 0-64, 0-42, 0-27, 0-17 and 0-85, 0-62, 0-35,0-23, 0-13 at 6-2, 2-7 and 0 7 cycles/degree respectively.To control for effects of possible side differences thenormal subjects adjusted the contrast with the variablegratings positioned first to the left and thereafter to theright side at each session. Contrast matching started at the

Contrast sensitivity Vertical, stationary, sinusoidalgratings were generated on a black and white televisiondisplay as previously described.7 The contrast sensi-tivity at threshold was determined monocularly byraising contrast from a subthreshold setting at a selectedspatial frequency until a grating pattern was faintly seen.The television monitor was masked to subtend 6 x 6degrees of angle at the eye, when viewed at a distance of2-5 m and sixteen frequencies were explored twice inrandom order. The contrast was adjusted by the experi-meter in steps of 2 dB within the contrast range 0-001 to0.9.

Suprathreshold apparent contrast was measured bypresenting two vertical, sinusoidal gratings side by side.For one eye television-generated grating with variablecontrast (see above) and for the other a non-variable,photographically produced grating was shown. Bothgratings had identical spatial frequencies, space-averageluminance about 80 cd/M2 and subtended 6 x 6 degreesat the eye. The non-variable photographic gratings wereproduced by photographing the television-generatedgratings at different contrast levels and spatial fre-quencies. The modulation characteristics of the colourdiapositives were checked by microdensitometry and theyhad a horizontally oriented sine-square light profile. Thephotographic gratings were projected by transilluminationand the space-average luminance of the projected gratingwas matched to that of the television-generated one byneutral density filters.

Procedure The observer's head was fixed by means of achin support 1-25 m in front of the gratings. The photo-graphic grating was presented for the eye with opticneuritis and the grating with variable contrast waspresented to the contralateral eye. The visual field for thetwo eyes were divided sagittally by placing a cardboardscreen between the eyes perpendicular to the frontalplane. Centres of the gratings were separated by an angleof 20° subtended at the eye. By this arrangement theobserver was forced to look at the grating with oneeye at a time when rapid eye changes during the matchingprocedure and smalleradaptation effects were anticipated.

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Suprathreshold vision in acute optic neuritis

highest spatial frequency and proceeded in order to thelowest one. At each spatial frequency all contrast stepswere presented in randomised order. Generally, a meanvalue for the two matches of the contrast for each pair

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Reference contrast Frequency Cycl/degFig 2 a-c Suprathreshold determinations in case EHplotted as the adjusted contrast (C) of thetelevision generated grating versus level of suprathreshold contrast (Co) of the non-variablephotographic grating. Range of matching in normal controls is indicated by the interrupted lines.Solid lines indicate the suprathreshold matching at different time intervals and visual acuity levelsduring the recovery from unilateral optic neuritis, 0 VA 0-1, * VA 0-6, A VA 0- 7, and * VA 1-5.d. CSF of the eye with optic neuritis at the same time intervals as usedfor suprathresholddeterminations (same symbols as above). 0 indicates the CSF of the contralateral eye. Dotted linesindicate the normal range of CSF in 10 normal observers. The normal observers are at approximatelythe same age as EH.

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230 Sjostrand, Abrahamssonmean value was calculated. Retesting within the same dayaccording to the procedure described above in two of thecases demonstrated a range of approximately 10%between the means of the two measurements. Eachsetting of contrast rarely took more than 10 seconds to

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Fig 3 a-c Suprathreshold determination in case TP. Plotted as the adjusted contrast (C) of thetelevision generated grating, versus level ofsuprathreshold contrast (C0) of the nonvariable photographicgrating. A-C shows the suprathreshold contrast matching for the three different frequencies 6-2, 2-7, and0 7 cycles per degree respectively. Range of contrast matching in normal controls is indicated by theinterrupted lines. Solid lines indicate the suprathreshold matching at different time intervals andvisual acuity levels during the recovery from optic neuritis, 0 VA 0-6, * VA 0 9, A VA 1O0.d. CSF of the eye with optic neuritis at the same time intervals as usedfor suprathresholddeterminations (same symbols as above). 0 indicates the CSF of the contralateral eye. Dottedlines indicate the normal range of CSF in 10 normal observers. The normal observers are atapproximately the same age as TP.


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between each spatial frequency tested.

Definitions The pattern contrast (C) is defined asLmax- Lmin,

C Lmax Lmin, where Lmax and Lmin denoteCLmax + 'minmaximum and minimum luminances respectively, Infigs 2 and 3 c denotes the pattern contrast of the televisiongenerated grating and c0 that of the photographic grating.

Results

THRESHOLD CONTRASTThe contrast sensitivity function (CSF) at threshold,that is, the reciprocal of the contrast threshold versusspatial frequency (fig 2d, range indicated by dottedlines) was similar to that obtained for normal sub-jects in a previous study7 with a peak value atapproximately three cycles/degree. The thresholdcontrast sensitivity of the eye contralateral to thediseased eye was within normal range in all caseswith isolated optic neuritis (fig 2d, 0). However,in the two cases with multiple sclerosis the contrastsensitivity of the contralateral eye was subnormal(fig 3d) in agreement with findings of earlierstudies.8 9The CSF of the eyes with acute, unilateral optic

neuritis was depresssed over the whole frequencyspectrum (figs 2 and 3d, filled circles) as describedpreviously.9 During recovery the extent of im-pairment of the CSF was correlated roughly tovisual acuity. In four of the five cases investigatedthe visual acuity recovered to 1-0 or above (table).The CSF, however, was still below normal range(figs 2 and 3d).

SUPRATHRESHOLD CONTRAST: NORMALSUBJECTSContrast matching with subjective equalisation ofsuprathreshold contrast was carried out twice (seemethods) on two separate occasions. The individualrange of these four measurements of adjustablecontrast was calculated for each spatial frequencyand in no case this range was above 0 03 . Measure-ments in all subjects at specific spatial frequenciesand contrast levels showed a range in matching of± 007. At the lowest contrast level, however, therange was less, that is, ± 0 05 as a maximal contrastdeviation from the preset level (indicated by in-terrupted lines in figs 2 and 3 (a-c). The differencebetween the two eyes was 0 03.

OPTIC NEURITISMeasurements of suprathreshold apparent contrastbetween the symptom-free and involved eyes ofpatients with acute optic neuritis demonstrated anabnormal contrast matching in all cases (table).

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Figures 2 and 3 (a-c) shows the contrast values ad-justed on the TV-screen (C) as a function of thereference contrast (CO) of the photographic gratingpresented to the eye with optic neuritis. In thesegraphs a normal contrast matching, that is, similarcontrast perceived by both eyes, fell between theinterrupted lines. In cases with unilateral acuteoptic neuritis a loss of apparent suprathresholdcontrast experienced by the affected eye occurred.The patient adjusted a contrast with his fellow eyebelow normal values. This loss of apparent contrastis illustrated in figs 2 and 3 (a-c) by solid linesfalling below the normal range (interrupted line).Typically, an attenuation of suprathreshold apparentcontrast was found for the involved eye for high(6-2 cycles/degree) and intermediate (2-7 cycles/degree) frequencies (figs 2, 3a and b). This relativecontrast loss increased at higher contrast levels.During the acute phase the loss was dramatic withadjusted contrast levels up to seven times below thatof the photographic grating. At a low spatialfrequency (0 7 cycles/degree) the contrast matchingshowed smaller or no deviations from normal(figs 2c and 3c). In two cases, contrast matching atlow spatial frequency was within normal limits(table, fig 2c), despite marked contrast loss athigher spatial frequencies. In two cases the apparentsuprathreshold contrast was above that of thecontralateral eye at a low spatial frequency althoughthreshold contrast at low spatial frequencies wasmarkedly impaired. During recovery of visualacuity the contrast matching improved graduallyat high and intermediate spatial frequencies. Whenan acuity level of 10 or above was reached themajority of the matching values was within normallimits (table; fig 2 (a-c), indicated by asterisks)in spite of a persisting attenuation of the thresholdcontrast sensitivity (table, fig 2d).

Discussion

The main finding of this study is that during theacute phase of optic neuritis the apparent supra-threshold contrast is reduced in the affected eyecompared to that of the unaffected eye. This relativeloss of apparent contrast experienced by the affectedeye was mainly restricted to high and mediumspatial frequencies. The loss was most marked at thehigher contrast levels. However, the contrastmatching of suprathreshold grating of low spatialfrequency was near normal unlike the marked lossin contrast sensitivity for the same grating atthreshold.Our study thus demonstrates that frequency-

specific losses occur in contrast sensation in acuteoptic neuritis. Innormal suprathreshold vision the gain


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Table Patient data, visual acuity and suprathreshold appar-ent contrast during the acute phase and lrecovery ofunilateral optic neuritis

Patient Age (yr) VA of the VA of the Inpairmnent of the apparent suprathreshold contrast of the affected eye atIsex alfected eye fe/loev eye different spatial frequencies and contrast levels

at differentphases of 0-67 cycl/deg 2-67 cycl/deg 6-2 cycl/degrecovery

> 0.35* 0-35 < 0-35t > 0-42 0-42 < 0-42 > 0-42 0-42 < 0-42

EH 30/F 0-1 1-5 0: 0 0 + 0 + 2 +0-6 0 0 0 0 0 0 + + 00-7 0 0 0 0 0 0 + 0 +1-5 0 0 0 0 0 0 0 0 0

TP 22/F 0-6 1-0 -l - -l -4-+ - -4-±-+ +0-9 + + O + -1-~~~+ + + + + +

0-9 ± 0 -4- + -I-- ± --1-0 + 0 +± 0 + -4- 0

L-OE 34/M 0-4 1.0 0 0 0 + + ++ + +L+ ++0-5 0 - - L -4- + ±++ -+ + +0-6 - - - + 0 + ++ +± ++1-0 0 - 0 0 0 0 0 0 0

GJ-R 32/F 0-4 1-0 0 0 0 ±+d + - L + ±±+0-5 0 0 0 + 4 -t- + + + +0-7 0 - 0 0 - 0 0 + 01-0 0 0 0 0 0 0 0 0 0

IB 66/F 0-1 10 - 0 ++ 0 + ++ ++ ++ ++0-8 -4- 0 0 ± 0 + - + --+ -

* > 0-35 or >0-42 denote the average at the two supratbreshold contrast levels above 0-35 or 0-42.t < 0-35 or < 0-42 denote the average at the two suprathreshold contrast levels below 0-35 or 0-42.+ 0 indicates contrast matching within normal range.+ indicates C) 50% of Co, -,- + C< 50% of Co, - C> Co.

that is the average slope of the linear relationshipbetween stimulus contrast and apparent contrast, isrelatively constant over the spatial frequency andsuprathreshold range used in this study.'7 Thefrequency-related losses are interesting in the light ofthe observation that the mechanisms involved inapparent contrast sensation of normal observers areas frequency specific as those involved in detec-tion.18 19 The findings in our study imply that theblurred vision in optic neuritis due to loss of apparentcontrast in suprathreshold vision of amedium or highfrequency grating might be cancelled by magni-fying the grating.8To our knowledge suprathreshold vision has not

been evaluated in optic nerve disease previously. Inamblyopia abnormalities of suprathreshold visionhave been reported.15 20-22 Hess and coworkers22described spatial distortions of grating patterns atsuprathreshold levels in amblyopia even thoughthreshold contrast sensitivity could be normal.Georgeson and Sullivan'3 reported that some astig-matic observers showed considerable suprathresholdcompensation for their orientation-specific neuraldeficit in threshold contrast sensitivity. They foundthat the attenuation observed at threshold (withoptimal optical correction) for gratings orientedalong the poor meridian was not reflected in supra-threshold apparent contrast for some of the astig-

matic observers. Therefore, it is not valid to gofrom threshold results to suprathreshold predictionsif the visual loss has a neural basis as shown by theirand our study. In the case of neural loss, allowingfor a recovery period, threshold may be affectedwithout any significant suprathreshold impairmentdue to a changed gain-setting mechanism as demon-strated in our study. However, when the visual losshas a pure optical basis, for example cataract, thethreshold impairment may be extrapolated tosuprathreshold levels.4During recovery following the acute phase of

optic neuritis a normalisation of suprathresholdvision occurred. In spite of a persisting abnormalityin threshold contrast sensitivity as demonstrated inthis and other studies9 10 12 the suprathresholdvision recovered in all patients in this study. Thisfinding may imply that some compensatory mechan-ism is active in suprathreshold vision. An alternativepossibility is that suprathreshold vision is mediatedby a different mechanism. At the same time ourobservations demonstrate that threshold contrastsensitivity tests are more appropriate for discoveringaxonal degeneration or demyelination in diseases ofthe visual system.8 9 Changesin suprathreshold match-ing not consistent with contrast sensitivity data hasbeen reported also for an amblyope by Ginsburg.15By monocular suprathreshold matching technique

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Ginsburg found evidence for complex gain systemsin an amblyope with over-compensation or under-compensation in different frequency channels atsuprathreshold contrast levels. Our finding of twocases with apparent contrast above that of the con-tralateral eye at low spatial frequencies in spite ofmarked threshold loss may be interpreted as anovercompensation, that is, the eye with neuritisrequired less contrast for matching. These dataindicate that much more complex gain systems fordifferent frequency channels might be present indisease than those found in normal observers.13

In this study few near-threshold contrast levelswere studied and our results only demonstratelosses at contrast levels above 0-15, that is, at highsuprathreshold levels. At contrast levels above 0-3Georgeson and Sullivan'3 have found in normalobservers a contrast constancy, that is, the supra-threshold apparent contrast is to a large extent in-dependent of the contrast sensitivity function and thegratings are seen in normal eyes as having anapparent contrast corresponding to its physicalcontrast. Testing of suprathreshold contrast levelsnear the threshold might have given different results,since Kulikowski23 has observed that for normaleyes suprathreshold apparent contrasts are equalonly when their suprathreshold contrast is defined asthe actual grating contrast minus its thresholdcontrast. This means, however, contrast constancyof patterns of higher contrast since at those levelsthe differences in contrast thresholds are negligible.Even though the lowest suprathreshold contrast inour study was 15 to 35 times the threshold contrastin normal observers this contrast level was nearthreshold in a few affected eyes with severelydepressed contrast sensitivity functions. For thesenear-threshold values some frequency dependenceof the suprathreshold contrast sensation might beanticipated in analogy with the finding of Georgesonand Sullivan'3 for normal observers.One major criticism of our method of contrast

matching is that effects from adaptation could occurfrom free inspection of high contrast gratings.'8 Tominimise the risk of adaptation the two gratings wereseparated by an angle of 200 subtended at the eyewhich forced the patient to look with one eyegenerally less than two to three seconds at a time.Furthermore, each setting of contrast rarely tookmore than 10 seconds to make-a period of timemuch shorter than that used for adaptation studies.18Interestingly enough, Raymond et a!24 have foundabnormally small adaptation effects in patients withmultiple sclerosis besides the finding of a reducedcontrast sensitivity function. On the other hand,Enoch et a125 have demonstrated visual fatigue in apatient with retrobulbar optic neuritis and probable

multiple sclerosis when exposed to high luminancelevels. Another complicating factor in suprathresholdmatching experiments is also that the affected eyehas to be compared to the fellow, symptom-free eye,which may be subclinically affected, as demonstratedin threshold contrast studies of patients with multiplesclerosis.8 9 In such cases an equalisation of supra-threshold matching between the two eyes do notimply normalisation. Studies are in progress in ourlaboratory to evaluate this by using a monocularmatching technique.15 In conclusion, dramaticrelative losses of suprathreshold contrast sensitivitymay occur during the acute phase of optic neuritis.Thus, for the diseased eye a high contrast gratingmay look identical to that of a low contrast presentedto the fellow eye. This might explain why patientswith acute optic neuritis often complain that objectsin the visual scenery of high contrast are dimmer andlose contrast.

This work was supported by the Swedish MedicalResearch Council (grant 02226) and Carmen andBertil Regners foundation. We are grateful to Drs RSekuler and L Frisdn for valuable advice andconstructive criticism.

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