Journal ofNeurology, Neurosurgery, and Psychiatry, 1979, 42, 407-412

Subtle disturbances of vision after optic neuritiselicited by studying contrast sensitivityR. L. ZIMMERN, F. W. CAMPBELL, ANDI. M. S. WILKINSON

From the Department of Neurology, Addenbrooke's Hospital, and The Physiological Laboratory,Cambridge University, Cambridge

S UMM A RY Eight patients with a subjective disorder of vision yet normal Snellen acuities afteroptic neuritis were shown to have an abnormal contrast sensitivity function in their affectedeye. It appears that certain disorders of vision are associated with an abnormality of thecontrast sensitivity function in spite of near normal visual acuity. Such an abnormality mayaffect pattern recognition without having an influence on Snellen acuity because of the highcontrast of the latter and its predominant association with the higher spatial frequencies.Contrast sensitivity function is thus the only tool available to study those aspects of visionwhich have remained impervious to other subjective tests of visual function.

'rhe determination of visual acuity in clinicalpractice has relied almost entirely on the use ofSnellen or similar charts, in which the letters usedare highly contrasted with their background andtheir sizes diminish from line to line so as topresent a progressively smaller visual angle to theeye. Such a measurement describes only a limitedaspect of visual perception, for it is common ex-perience that the visibility of objects depends notonly on their size but on their relative brightnesswith respect to their background. The relationshipbetween luminosity of object and background maybe expressed precisely as a contrast measurementand the ability of the visual system to see andanalyse objects and patterns may be consideredin terms of contrast as well as size.The study of this relationship can be carried out

conveniently using sinusoidal gratings of differentcontrasts and spatial frequencies (Campbell andMaffei, 1974). These are repetitive bar patternswhere the luminance of the dark and light barsare varied in a sinusoidal fashion. The spatialfrequency of such a pattern is defined by the num-ber of alternating bars subtended by one degree ofvisual angle at the eye and the contrast by theluminance differences of dark and light barsdivided by the sum of their luminances. The inter-

Address for reprint requests: Dr R. L. Zimmern, Departmentof Neurology, Addenbrooke's Hospital, Hills Road, CambridgeCB2 2QQ.Accepted 26 October 1978

action of size and contrast in the human visualsystem may be studied psychophysically by usingsuch gratings to determine the threshold contrastnecessary for grating detection at different spatialfrequencies. The reciprocal of the threshold con-trast is known as the contrast sensitivity and theplot of contrast sensitivity against spatial fre-quency is the contrast sensitivity function. Figure1 shows a grating varying in spatial frequencyalong the horizontal axis and varying in contrastalong the vertical axis. The junction between thevisible and invisible parts of the grafting definesthe contrast sensitivity function.The importance of contrast sensitivity is related

to modern ideas concerning mechanisms of patternrecognition. Fourier showed that any waveformcould be separated into sinusoidal components ofdifferent frequencies and amplitudes. His theoremwas applied successfully by Helmholtz to thephysiology of hearing and allowed an understand-ing of how complex sounds might be analysed intotheir respective simple frequency components.Only in recent years has such an analysis beenapplied to the visual system (Campbell, 1973).

Microelectrode studies have shown that cellsexist in the visual system which respond to sinu-soidal gratings of a limited range of spatialfrequencies (Enroth-Cugell and Robson, 1966; Cle-land et al., 1971; Campbell et al., 1969). Thesestudies, which are now extensive, have enableda theory of perception based on the concept of fre-

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Fig. 1 Grating with spatial frequency varying along horizontal axis and clontrast sensitivity along verticalaxis. The junction between the visible and invisible parts of the grating defines the contrast sensitivityfunction.

quency specific channels in the visual pathways.The application of Fourier theory was to suggestthat complex visual information could be carriedin these frequency specific channels in much thesame way that complex harmonies in the domainof hearing are carried in the auditory system bysimilar frequency channels. In man, the existenceof these channels has likewise been shown by theuse of appropriate psychophysical techniques.Experiments in which contrast sensitivity functionswere constructed using square-wave, rectangular,and saw-tooth rather than sinusoidal gratings haveproduced results to be as calculated by Fouriertheory (Campbell and Robson, 1968).The normal contrast sensitivity function may,

therefore, be seen as the envelope of the turningcurves of the different spatial frequency specific

channels with respect to their ability to respondto different contrasts. Those channels with a fre-quency of approximately 3 c/deg are seen to bemost sensitive while channels on either side ofthis frequency are seen to be progressively lesssensitive. Damage to the different spatial fre-quency channels will lower their sensitivities andwill be detected as an abnormality of the contrastsensitivity function. Abnormal vision may beconstrued to result from damage to some or allthe spatial frequency channels if the concepts ofFourier theory are followed. Such abnormal visionmay be detected as an abnormal contrast sensi-tivity function but need not result in an abnormalSnellen acuity.The relationship between the Snellen acuity and

the contrast sensitivity function is complex but

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Subtle disturbances of vision after optic neuritis elicited by studying contrast sensitivity

appears to be concerned with mechanisms at thehigher end of the spatial frequency range. Thusabnormalities of the Snellen acuity would not beseen if low or medium frequency channels weredamaged or if the rise in the contrast theshold(corresponding to a reduction in contrast sensi-tivity) in the high frequency channels did notexceed the high contrast of the Snellen figures.An abnormality in the contrast sensitivity func-

tion has been shown in a heterogeneous group ofpatients with cerebral lesions and a complaint ofblurred vision, (Bodis-Wollner and Diamond,1976) and also in a number of patients with mul-tiple sclerosis (Regan et al., 1977) some of whomshowed no abnormality of visual function onstandard clinical tests. This preliminary com-munication reports a study of eight patients withoptic neuritis or multiple sclerosis who com-plained of a disturbance of vision in the presenceof good Snellen acuities.

Patients and methods

Eight patients took part in the study. Six had well-documented histories of optic neuritis in one eyeand one had at different occasions such episodesinvolving each of her eyes in turn. All seven hadrecovered from the acute episode in that theirvisual acuity was 6/9 or better but all still com-plained of some subjective disturbance of visionin the affected compared with the unaffected eye.Of these seven patients six had other symptomsand signs of multiple sclerosis. The eighth patientpresented with a paraparesis but had complainedof a visual disturbance in his left eye over thepreceding three years in spite of normal Snellenacuities. Control subjects were members of theNeurology and EEG Departments at Adden-brooke's Hospital.

In all these patients visual acuity was assessedby the use of Snellen charts. Colour vision wasdetermined using Ishihara pseudo-isochromaticplates, and four mistakes or greater were taken

to be consistent with an abnormality of colourperception. The appearance of the optic discs wasnoted and a relative afferent pupillary defect wasdetected by the use of the "swinging torchlighttest" (Levitin, 1959). Visual evoked potentialswere obtained using the method of Halliday et al.(1972). The results of these ophthalmic investiga-tions are shown in the Table.

Contrast sensitivity was determined using amethod based on that of Schade (1956). Verticallyorientated stationary sinusoidal gratings were dis-played on the screen of a cathode-ray tube usinga waveform generator. With suitable synchronis-ation of the time base different spatial frequenciescould be displayed. The contrast of the gratingpattern was varied by adjusting the modulationvoltage using a logarithmic step attenuator. Con-trast was defined as Lmax-Lmin/Lmax+Lmin whereLmax and Lmin are the luminances of the light anddark bars respectively. The screen was set up witha base contrast of 0.33 with zero attenuation. Themean screen luminance was 100 Cd/M2 and wasindependent of the contrast and of the spatialfrequency of the grating being displayed. Thescreen of the cathode-ray tube was covered by apiece of white cardboard measuring 750X500 mmand having a central aperture 250X200 mm. Nospecial lighting was directed at the cardboard andexperiments were conducted in conditions ofordinary room lighting which was kept constantfrom experiment to experiment. At spatial fre-quencies of 2 c/deg or above, measurements weretaken at a distance of 2280 mm, and at 1 c/deg or

below at 570 mm. The spatial frequencies usedwere 8 c/deg, 6 c/deg, 20 c/deg, 4 c/deg, 10 c/deg,2 c/deg, 15 c/deg, 1 c/deg, 0.4 c/deg, 0.2 c/deg,and 0.6 c/deg, all presented in the order shown.No formal refraction was carried out but trial

lenses ranging from -0.5 to +0.5 dioptres were

used if the patient thought subjectively that theseimproved acuity. Contrast thresholds were deter-mined by the subject who adjusted the attenuatoruntil a contrast was reached at which some form

Table Results of ophthalmic investigations

Patient Age Visual acuity* Colour vision Afferent pupillary Pallor Visual evoked(yr) (affected eye) defect response

HR 50 6/9 Abnormal + + DelayedCH 38 6/6 Normal Equivocal No DelayedCB 21 6/6 Normal + + DelayedMJ 30 6/6 Abnormal + + DelayedSS 31 6/6 Abnormal Equivocal Equivocal DelayedBG 45 6/6 Abnormal + Equivocal DelayedVA 29 6/6 Normal No + DelayedMD 23 6/6 Normal No No Delayed

*The visual acuity of the "unaffected" eye was 6/6 in all the patients.

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of stimulus could just be detected on the screen.Ten observations were made at each spatial fre-quency, and the results were fed into a PDP8 com-puter which derived, from the attenuation voltageand the base contrast, the mean contrast sensitivity.

Results

The contrast sensitivity functions of five controlsubjects were obtained from which a mean con-trol curve with 99% confidence limits was derived.The contrast sensitivity function of each of thepatients' eyes was individually compared with thecontrol function. This was done by plotting, ateach spatial frequency, the ratio of the testcontrast sensitivity to that of its control. Thisresultant attenuation function has been labelled,by Bodis-Wollner, a visuogram.

Figure 2 shows the normal contrast sensitivityfunction derived from the five control subjects with

1%, 5%, 95% and 99% confidence limits. Thedotted contrast sensitivity function is that of theaffected eye of one patient (MJ) and serves as anexample of an abnormal contrast sensitivity func-tion. Above this is the visuogram for this patientplotted by taking the ratio of her contrast sensi-tivity function to that of the mean control curve.Figure 3 shows the visuograms of the eightpatients. The dotted line is the visuogram from theaffected eye and the continuous line is the visuo-gram from the "unaffected" eye. The line bound-ing the shaded area represents the first percentileof the normal contrast sensitivity function ex-pressed in the form of the visuogram.

It can be seen that the visuograms of the un-affected eyes of all patients except one (SS) laywithin or above the shaded area. She had multiplesclerosis and was the most severely affected of thepatients tested. She also made three errors in theIshihara plates with her unaffected eye while no

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Fig. 2 Mean contrast sensitivity functionfrom five normal subjects plotted as the

99% 50th percentile with 95% and 99%confidence limits plotted as first, fifth,95th and 99th percentiles. Dotted curve isthe contrast sensitivity function for theaffected eye of subject MJ. Thevisuogram above shows the ratio of MJ'scurve to that of the mean control

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Subtle disturbances of vision after optic neuritis elicited by studying contrast sensitivity

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Fig. 3 Visuograms of eight patients with optic neuritis. *0 =right eye *=left eye.

Dotted line represents the eye involved by optic neuritis. Continuous line representsthe "unaffected" eye. Shaded area represents the first percentile of the normalcontrast sensitivity function plotted as a visuogram.

mistakes were made by the unaffected eyes of theother patients. One can, therefore, conjecture thatshe had subclinical involvement of her "un-affected" optic nerve. The visuograms of both theaffected and unaffected eyes of patient VA laywithin the shaded area but it is clear that thevisuogram from the affected eye was constantlybelow that from the unaffected eye. Patient MD,who had optic neuritis in both eyes, had bilaterallyabnormal visuograms.

Discussion

Our results confirm those of Regan and his col-leagues (1977) that there are patients with multiplesclerosis who have normal visual acuities and yetwho complain of imperfect or "washed out"vision and that these patients may have an abnor-mal contrast sensitivity function. Their patientsfell into five groups: (1) those with no abnor-mality in their contrast sensitivity function; (2)those with a similar loss at all spatial frequencies;(3) those with a preferential loss at high or atmedium and high spatial frequencies; (4) thosewith a loss restricted to medium spatial fre-quencies; (5) those with a restricted low spatialfrequency loss. Our limited study shows examples

of all these groups except the fifth. Regan et al.(1977) do not give any details of the neuro-ophthalmological findings in their patients butentitle their paper "Visual acuity and contrastsensitivity in multiple sclerosis-hidden visual loss.An auxiliary diagnostic test." Our data, sum-marised in the Table, show that all our patientshad some form of neuro-ophthalmological abnor-mality to point to an optic nerve disorder. Moreinformation is necessary to establish whetherstudies of the contrast sensitivity function do con-stitute an auxiliary diagnostic test in showing upan abnormality of optic nerve function not shownby the other clinical tests.

It does appear from the results of this study andothers that certain disorders of vision are associ-ated with an abnormality of the contrast sensitivityfunction in spite of near normal visual acuities. Ifthe visual cortex acts as a spatial frequencyanalyser, as has been suggested (Maffei andFiorentini, 1972, 1973), an abnormal contrastsensitivity function reflecting disturbances in cer-tain spatial frequency channels will lead to faultyvisual information processing. Such an abnor-mality may greatly affect pattern recognition yetnot have an influence on Snellen acuity becauseof the high contrasts of the latter and its predomi-

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nant association with the higher spatial fre-quencies. The contrast sensitivity function is thusthe only tool available to study those aspects ofvision, in particular low and medium frequencychannels and patterns of low contrast, which haveremained impervious to hitherto available testsof visual function.We believe that contrast sensitivity studies hold

great promise in this respect, not only as a possiblediagnostic aid but also for the relevance that ab-normal findings may have to an understanding ofnormal visual physiology.

We wish to thank Dr M. F. T. Yealland for per-mission to study patients under his care, Dr RobertHess and Dr A. P. Ginsburg for helpful discussion,Miss Peggy Hall and the staff of the EEG Depart-ment, Addenbrooke's Hospital, and Mr Clive Hoodof the Physiological Laboratory, Cambridge fortechnical assistance.

References

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Campbell, F. W. (1973). The transmission of spatialinformation through the visual system. In Neuro-sciences Third Study Programme, p. 95. Edited byF. Worden and F. 0. Schmitt. MIT Press: Cam-

bridge, Massachusetts.Campbell, F. W., Cooper, G. F., and Enroth-Cugell,

C. (1969). The spatial selectivity of the visual cellsof the cat. Journal of Physiology, 203, 223-235.

Campbell, F. W., and Maffei, L. (1974). Contrast andspatial frequency. Scientific American, 231, 106-114.

Campbell, F. W., and Robson, J. G. (1968). Appli-cation of Fourier analysis to the visibility of grat-ings. Journal of Physiology, 197, 551-566.

Cleland, B. G., Dubin, M. W., and Levick, W. R.(1971). Sustained and transient neurones in the cat'sretina and lateral geniculate nucleus. Journal ofPhysiology, 217, 473-496.

Enroth-Cugell, C., and Robson, J. G. (1966). The con-trast sensitivity of retinal ganglion cells of the cat.Journal of Physiology, 187, 517-552.

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Levitin, P. (1959). Pupillary escape in disease of theretina or optic nerve. Archives of Ophthalmology,62, 768.

Maffei, L., and Fiorentini, A. (1972). Processes ofsynthesis in visual perception. Nature, 240, 479-481.

Maffei, L., and Fiorentini, A. (1973). The visualcortex as a spatial frequency analyser. Vision Re-search, 13, 1255-1267.

Regan, D., Silver, R., and Murray, T. J. (1977). Visualacuity and contrast sensitivity in multiple sclerosis:hidden visual loss. Brain, 100, 563-579.

Schade, 0. H. (1956). Optical and photoelectricalanalog of the eye. Journal of the Optical Societyof America, 46, 721-739.

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