contrast blurring - bmj

Journal of Neurology, Neurosurgery, and Psychiatry 1983;46:1023-1030

Contrast vision and optic neuritis: neural blurringROBERT F HESS

From the Physiological Laboratory, University of Cambridge, and the Department of Neurology,Neurosurgery and Psychiatry, Addenbrookes Hospital, Cambridge, UK

SUMMARY In order to understand the vision of patients with long standing optic neuritis, contrastperception was analysed in some detail for three patients with uniocular anomalies. Contrastdetection and contrast matching experiments each demonstrate anomalies in contrast processingfor eyes with optic neuritis. In this regard, optic neuritis differs from all other visual anomalies sofar investigated where the suprathreshold deficits (from matching experiments) are slight com-pared with those measured under threshold conditions (from detection experiments). Contrastdiscrimination is also impaired to a mild degree in optic neuritis but this cannot be predicted onthe basis of the matching results. These results bear upon the currently proposed models forcontrast coding in the normal visual system as well as the nature of the underlying pathology inoptic neuritis.

Over the past decade our concept of the type ofvisual loss that occurs in patients with optic neuritishas been greatly clarified by the measurement ofcontrast thresholds with sinusoidal gratings of dif-ferent bar width or spatial frequency. Followingfrom the original work of Bodis-Woilner' on cere-bral lesions, other workers23 have shown that notonly can thresholds for low spatial frequency stimulibe affected independently of acuity but thresholdsalso can be raised for only a limited band of inter-mediate spatial frequencies.

Although this threshold information is interestingfor reasons of classification and diagnosis it fails toanswer questions relating to the visual perception ofthese patients because it does not directly assess theperception and processing of suprathreshold con-trast information of which everyday images arecomposed. The fact that threshold and supra-threshold contrast processing can differ is evidentfor normal vision45 and amplified in the case of thedevelopmental anomalies (amblyopia) of vision.6 Ineach case (normal or amblyopic) conditions can befound for which thresholds are raised yet supra-threshold performance is normal.

In order to gain more insight into the visual per-ception of patients with optic neuritis and not justtheir abilities for threshold detection, contrast pro-

Address for reprint requests: Dr RF Hess, Dept of Physiology,Cambridge CB2 3EG, UK.

Received 17 March 1983 and in revised form 14 May 1983.Accepted 2 June 1983

cessing above threshold was investigated with twodifferent but complimentary techniques. First, con-trast matching was measured between the normaland anomalous eye of patients with optic neuritis.Secondly, incremental contrast discrimination wasexamined over a wide range of stimulus contrast fornormal and anomalous eyes.We have sought a better understanding of the vis-

ion and thus the visual defect in optic neuritis forstimuli whose contrast is at and above threshold. Werelate these findings in optic neuritis to each of thetwo current psychophysical models of how contrastis processed in the normal visual system.45 To thisextent, this report differs in its approach from that ofSjostrand and Abrahamsson7 who reported on therecovery of suprathreshold contrast perception inoptic neuritis. We have concentrated on the remain-ing deficit rather than the recovery that characterisesthe initial attacks. We have used more establisheduniocular cases and examined in more detail con-trasts just suprathreshold. The table gives the clini-cal details of the patients studied.

Methods

ApparatusVertical sinewave gratings (temporal frequency = OHz)were generated analogically or digitally and displayed oneach half of a specially constructed 20 cm x 30 cm videodisplay (P31 phosphor). The spatial frequency and contrastof each of these waveforms could be independently varied.Contrast was linearly related to input voltage up to 90%contrast. The mean luminance of each was equal and set to

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Table Clinical details ofpatients studied

Patient Age Diagnosis Length of Visual Ishihara RAPD Optic Visual Contrast(yr) history acuity test no disc field threshold

(months) of errors loss

KT 34 Unilateral optic 6 6/24 None No Normal Normal Localisedneuritis mid-frequency

lossMM 49 Unilateral optic 12 6/60 7 Yes Pallor Central Mainly

neuritis from (visual) scotoma mid-frequencymultiple sclerosis loss

JL 46 Unilateral optic 18 6/6 1 No Pallor Normal Low pass lossneuritis

SS 28 Unilateral optic 24 6/12 6 Yes Pallor Normal Generalisedneuritis spatial loss

IW 20 Bilateral optic 24 6/60 10/4 Yes Bilateral R & L Generalisedneuritis from (visual) R & L R/L pallor central spatial lossmultiple sclerosis scotoma

200 cd/m2. The subject viewed these gratings from a dis-tance of 114 cm (100 field size) such that, by the use of apartition, the gratings were seen dichoptically. A slowlyrotating sectored disc alternately occluded one eye andsimultaneously presented a grating to the other eye everysecond. Furthermore, the gratings were presented for an 8second interval every 20 seconds in this mode. This switch-ing from grating to mean luminance was used to avoiddifferential adaptation effects at higher contrasts.8 Thesubject either made a series of threshold settings or supra-threshold matches during these exposures. A tone signal-led the beginning of the 8 second test period.The method of adjustment (N = 5) was used for all

matches. At first the subject was carefully refracted forametropia and a viewing distance of 1 metre. The spatialfrequencies were then subjectively matched for normal andanomalous eyes. Contrast thresholds were then measuredunder the stimulus conditions already discussed and con-trast matches at 3 dB steps (in random order) were thenmade up to 90% contrast for the two objectively equalspatial frequencies. A grating of present contrast (referredto as the standard) was always presented to the anomalouseye. Racalibrated Kodak neutral density filters in goggleswere used to reduce the luminance (of both fields) andangular field size was varied by changing distance. Allresults on the patients used were rechecked on at least onesubsequent occasion.

Contrast discrimination experimentsThese experiments involved a successive, two alternativeforced choice procedure for both the measurement of con-trast threshold and the contrast necessary to determinethat two suprathreshold gratings were different in contrast.In the first procedure the subject was presented (threshold)with two intervals each of 500 milliseconds (time Gaus-sian), one of which contained a sinewave grating. TheQuest psychophysical procedure was used9 which involveda staircase method driven from maximum likelihood esti-mates. Sixty trials were run for each threshold estimate.

In the contrast discrimination experiments the same pro-cedure was used except that two gratings of the same spa-tial frequency were presented and the task was to choosewhich interval contained the higher contrast grating. Aminimum of 60 trials were run for each condition. A PDP11/20 computer presented the stimuli and collected

responses. The normal and fellow anomalous eyes werealways alternately tested at each condition. The experi-ments were always repeated on another occasion.

Results

A CONTRAST MATCHINGIn fig 1 the results for a normal inexperiencedobserver are shown for equating the contrast of sev-eral spatial frequencies between eyes. Each datumrepresents the average of five settings with verticallines indicating + 1 standard deviation of the set-tings. In a number of cases this was less than thesymbol size used. It is evident that for spatial fre-quencies between 0*3 and 10 c/deg equating the con-trast of identical spatial stimuli each presented to adifferent eye can be performed in a proportional(fitting a 450 line) and accurate manner (small SD).

Results for three of the cases of optic neuritisstudied are displayed in figs 2-4. In fig 2 contrastmatching was performed between the normal andfellow affected eye of patient (JL) (unilateraldeficit). The threshold contrast loss which is shownin the figure inset is seen not to vary with spatialfrequency. When contrast was equated between theeyes of this patient at three different spatial fre-quencies, functions were obtained each having slopebut displaced by differing amounts from the normalmatching line (solid line). The amount of this verti-cal displacement equalled the threshold deficit (halffilled symbols on these functions are threshold esti-mates). Such a displacement represents a constantratio change in perceived contrast by the anomalouseye. For the 4 c/deg stimulus the perceived lumi-nance and colour were adjusted to be equal betweeneyes (V) and this is seen not to affect the perceivedcontrast (circles).

Fig 3 shows results for a similar experiment con-ducted on another case of unilateral optic neuritishaving a specific mid-frequency defect in thresholdsensitivity (KT) of the type first reported by Regan,

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0-003 0.003 0003 0-003 0 01 0-03 0 1 0-3Contrast of standard ( right eye )

Fig 1 Contrast matching results are displayed for a norrnal observer for a range ofspatial frequencies. Astandard contrast was presented to the right eye and matched by varying the contrast ofan identical patternshown to the left eye. For normal eyes in optimal focus, contrast can be matched accurately. Vertical barsindicate + one standard deviation.

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Fig 2 Contrast matching results for a case of unilateraloptic neuritis (JL). Three spatial frequencies were

investigated. For each frequency, a standard grating was

presented to the anomalous eye at each ofa number ofbasecontrasts. An identical but variable stimulus was presentedto the fellow normal eve and equated for contrast. The scalesare logarithmic and the halffilled symbols representdetection thresholds for normal and anomalous eyes foreach stimulus. For the 4 cldeg stimulus the luminance andcolour differences perceived by the anomalous eye were

carefully eliminated. This does not affect theresultant contrast match. Results for a normal observerwould lie along the heavy diagonal line. Inset in the figureare the detection threshold results (low pass loss) with thethree spatial frequencies investigated marked by arrows.

Vertical error bars indicate + I SD. In all cases a paralleldisplacement occurs in suprathreshold matching.

Optic neuritisKT

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0-003 0 01 0 03 0-1 0 3 0 1Contrast of standard (anomalous eye

Fig 3 Contrast matching results for a case of unilateraloptic neuritis (KT). Three spatial frequencies wereinvestigated. For each, a standard grating was presented tothe anomalous eye at each ofa number ofbase contrasts. Anidentical target but variable contrast was presented to thefellow normal eye and matched to the standard. The scalesare logarithmic and the halffilled symbols are detectionthresholds. Results for a normal observer would fit along thesloping diagonal line. Inset in the figure are the detectionthreshold results (band pass loss) with the spatialfrequencies position of the three gratings used in thematching experiment indicated. Spatial stimuli were chosento correspond with the pit and shoulders ofthe notch loss indetection sensitivity. Vertical error bars represent + I SD. Aparallel shift in suprathreshold sensitivity is observed for allfrequencies.

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Optic neuritis Silver and Murray.2 In this case, contrast thresholdsMM *,05c/d were evenly displaced in one eye for all spatial fre-

0 3 quencies higher and lower than the threshold notchloss (centred at 5 c/deg). Similar results are seen for

>1 targets whose spatial frequency represent the shoul-ders of the threshold notch loss and a frequency

&01$ 4' representing the pit of the threshold notch loss.0 / Results similar to those seen in fig 2 are displayed003 / 4 * , for another unilateral optic neuritis for three differ-

2i00 MM0 / ent spatial frequencies (fig 4).cz

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5c/d > &+' '*cIn fig 5 the characteristic loss in contrast percep-0.o1- / we 10 * tion (parallel displacement) is seen to occur inde-

. .pendently of field size. As the field size is extended1Sptil 6frequency(c60kg) from 2 x 20 to 16 x 160, the overall deficit

0 003 0 03 diminishes but the form of the contrast loss remains0003 001 0-03 01 03 unchanged. Similarly as luminance is reduced byContrast of standard (anomalous eye interposing a neutral density filter before both normal

Fig 4 Contrast matching results for a case of unilateral and fellow anomalous eyes, threshold and supra-optic neuritis (MM). Three spatial frequencies were threshold function is seen also to remain unchangedinvestigated. For each, a stantdard grating was presented to in form but with a diminished contrast range (fig 6).the anomalous eye at each of a number of fixed contrasts.An identical but variable (contrast) stimulus was presented B CONTRAST DISCRIMINATIONto the fellow normal eye and equated for contrast. The scales The results of comparing contrast discriminationare logarithmic and the half ifiled symbols represent

s. tdetection thresholds. Results for a normal observer would between normal eyes and those sufferIngfrom OptiClie along the heavy diagonal line. A parallel shift ofthe data neuritis are displayed in figs 7 and 8. In fig 7,is seen to occur at each spatial frequency. Inset in the figure observer SS exhibited a contrast deficit for only loware the detection threshold results (overall broad band loss) spatial frequencies (<1 c/deg). In each of the figureswith the spatial frequencies used for matching indicated. the contrast thresholds for normal and affected eyesVertical eror bars represent ± I SD. is indicated by unfilled and filled arrows respec-

tively. These thresholds were measured using an

Field sizeJL (Optic neuritis) /

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(}003 001 003 0-003 0-01 0-03 ao03 001 003 01 03 1Contrast of standard (anomalous eye)

Fig 5 Contrast thresholds (halffiled symbols) and suprathreshold matches (open symbols) are displayedfor a uniocular case of optic neuritis. The characteristic forn of the suprathreshold loss (parallel shift ofunity slope) is independent of the field size ofthe grating stimulus out to 16° x 160. The magnitude ofboththe threshold and suprathreshold loss increases slightly for the small field size. Each stimulus was centrallyfixated. Vertical error bars represent + 1 SD. JL has an even pass threshold loss.

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Contrast vision and optic neuritis: neural blurring

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J L Optic neuritis4 c/deg

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Fig 6 Contrast thresholds (halffiled symbols) andsuprathreshold matches (open symbols) are displayed for a

uniocular case of optic neuritis. Neither the characteristicform of the suprathreshold loss function nor its magnitudedepend upon the mean luminance of the stimuli. A paralleldisplacement of the same magnitude is seen for a widevariation (10) ofspace-averaged luminance. 0 ND refers tothe normal luminance of200 cd/M2, whereas 4 ND refers toa luminance of0.02 cd/r2. Contrast thresholds for each eye

vary with luminance in a systematic but synchronous way.

The vertical error bars represent + I SD. This observerdisplayed only a slight loss of threshold sensitivity.

identical technique to that for contrast discrimina-tion. The results of fig 7 indicate that when onlyrelatively slight deficits occurred for threshold detec-tion no measurable loss in discrimination for incre-mental (or decremental) suprathreshold stimuli wasfound. The results for the affected eye and normalfellow eye are similar and were well fitted by astraight line of almost unit slope for 4 c/deg andslightly less than unity for 0-5 c/deg.

In fig 8, observer KT had unilateral optic neuritissimilar to SS whereas subject IWs condition was

bilateral. In this case (IW) the anomalous results are

compared with those from an age matched, inex-perienced normal observer. Contrast discriminationwas anomalous for the affected eyes. The anomalousresults were well fit by parallel straight lines of near

unit slope, and showed that at all contrast levels theanomalous eye required the same, proportionatelylarger increment in contrast than normal for correctdiscrimination. The threshold deficits that are indi-cated for the normal and anomalous eye withunfilled and filled arrows show little or no corres-

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pondence with the magnitude of the contrast dis-crimination abnormality. In the case of SS (fig 7)and KT (fig 8) the contrast matching results dis-played a parallel shift at all contrast levels asdescribed earlier. The dashed straight lines in figs 7and 8 represent the normal discrimination resultsshifted to lower contrast levels by an amount equalto the contrast matching anomaly (at and abovethreshold) for the anomalous eye. This dashed linenow allows a comparison between normal andanomalous eyes for contrast discriminations aboutsubjectively equivalent base contrasts. For example,if an anomalous (figs 2-5) eye perceives all contrastsa factor of two below their actual level then contrastdiscrimination thresholds should only be validlycompared at equivalent subjective base contrasts.Shifting the normal discrimination results along theX-axis by a factor of two achieves this equivalenceof base contrasts.

Discussion

These matching results suggest that the lossesobserved for threshold stimuli are just as pro-nounced at suprathreshold levels. At first glancethese results seem to be at odds with the conclusionsof Sjostrand and Abrahamsson7 who reported thatin optic neuritis for mid-high spatial frequencies"the relative contrast loss increased at higher contrastlevels". However these authors plotted their resultson linear coordinates whereas in the present studythey have been plotted on logarithmic coordinates.A closer inspection of their results reveals that thecontrast perceived by the anomalous eye is a con-stant ratio below that of normal in agreement withthat found in the present study. Since the perceivedcontrast varies as the logarithm of the physical con-trast (observe fig 3 of Campbell,'0 where alogarithmic decrease in physical contrast appears tobe perceptually linear), this finding is thus interpret-able in terms of an abnormality that affectsthreshold and suprathreshold levels with equal per-ceptual weight. The assertion by these authors thatlow spatial frequencies behave differently from midto high frequencies is not supported by the 0*5 c/degresults displayed in fig 4. However, more informa-tion is required to answer this point. Thus opticneuritis is one of the only conditions so far describedin which there is a true loss of "contrast sensitivity"in its more general sense. Contrast perception forthe developmental anomalies of vision (strabismic,anisometropic and deprivation amblyopia) as well assome retinal pathology (Hess unpublished) showstriking recruitment above threshold. In these con-ditions, threshold losses far outweigh those found forsuprathreshold stimuli.6 This contrast loss in optic



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Fig 7 Discrimination results for incremental changes in contrast are displayed for the normal(open symbols) and fellow anomalous eye (filled symbols) of observer SS who exhibiteduniocular optic neuritis. Results for two spatial frequencies are displayed. The discriminationresults are normal, equal in both eyes and well fitted by a line ofunit slope. Filled and unfilledarrows mark the detection thresholds of the anomalous and normal eyes respectively asmeasured with the same 2 AFCprocedure. The dashed line represents a parallel displacement ofthe line best fitting the normal results to lower base contrasts by an amount equal to thedifference in contrast matching for the normal and anomalous eyes (see text). Standarddeviations are never greater than 1-5 times the symbol size.

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Fig 8 Discrimination results for incremental changes in contrast are displayed for the normal (unfilledsymbols) and fellow anomalous eyes (filled symbols) ofa case ofunilateral optic neuritis (KT) and one ofbilateral optic neuritis. In the bilateral case, the results are compared with those from an age matched

normal observer (unfiled symbols). The discrimination results are anomalous in all cases and displacedwith a constant slope. The filed and unfiled arrows represent the detection thresholds for the anomalousand normal eyes respectively as measured using the same 2 AFCprocedure. Standard deviations are never

greater than 1 5 times the symbol size. The dashed line presents a parallel displacement ofthe line ofbest fitto the normal results to lower base contrasts by an amount equal to the difference in contrast matching forthe normal and anomalous eye (see text).

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Contrast vision and optic neuritis: neural blurringneuritis can be thought of as neural blurring becauseit is quantitatively similar in its effect at any onespatial frequency (but not necessarily across spatialfrequency) to that of optically defocusing thestimulus. This analogy also helps us understand atleast some aspects of visual perception of thesepatients and why in particular they report that theirvision appears "washed out", "faded" or " blurred".

It is interesting to note that the form of the con-trast loss does not depend on field size or luminance.Hess and Plant"' have found that the effect of tem-poral frequency variation on threshold losses inoptic neuritis, can be mimmicked in normal obser-vers by artificial scotomata. They have suggestedthat (as seems likely from the pathology) patchyinvolvement of the optic nerve, and hence visualfield, might result in islands of relatively preservedfunction which would account for their findings. Thepresent results suggest that the effect of this patchydisturbance on perception does not vary with con-trast or mean luminance and does not vary greatlywith eccentricity. There is, however, some variationwith field size as would be predicted from a nonhomogeneous disorder (fig 7). In other words, thoseabnormal regions of the visual field are character-ised by a reduced gain (divisive loss) such that theyrepresent absolute scotomata for threshold teststimuli and relative scotomata for suprathresholdtest stimuli.The contrast discrimination results are only

slightly anomalous compared with the steady rateanomaly seen from matching experiments. The con-trast discrimination anomalies in optic neuritis arenot simply explained by the loss of subjective con-trast that has already been described in the first sec-tion of this paper. For example, the contrast dis-crimination results of normal eyes and those withoptic neuritis do not match even when compared atsubjectively equivalent base contrasts (for example,by displacing the normal discrimination function tolower base contrasts by an amount equal to the lossof perceived contrast in optic neuritis). These resultssuggest that either contrast discrimination is betterthan normal in optic neuritis or the adjustment toequate base contrast in terms of their subjectiveappearance is invalid. The latter suggestion seemsthe more likely. This in turn implies that matchingand discrimination have quite different and inde-pendent physiological substrates, a conclusion alsoseen in other results" 12 in which contrast discrimi-nation in the recruiting region of amblyopic contrastmatching functions is never better than normal.

Neither of the two models of contrast coding fornormal vision are suitable for the description ofthese results in optic neuritis. Kulikowski5 proposeda model in which the subjective contrast (Cs) was

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directly proportional to the physical contrast (C)minus the contrast threshold (KD). That is: Cs X logC - KD. Georgeson and Sullivan,4 on the otherhand, postulated that subjective contrast for stimulihaving different thresholds was equated above acriterion value, that is subjective and physical con-trasts are related as follows: if C < 0-4 then Cs = logC.The present results however, are well described

by a divisive relationship that is: Cs = log C/KR,where KR is the ratio of contrast thresholds.

In an attempt to explain the contrast recruitingresponses that typify contrast perception for thedevelopmental anomalies of vision (amblyopia) analternative proposition'2 has been proposed to thatof Georgeson and Sullivan4 or Kulikowski.5 Thesuggestion involves the notion of more than onecontrast "channel". In its simplest form twomechanisms, one responding to lower contrasts(more sensitive) than the other. Such a model whichhas some neurophysiological support in the findingsof Shapley, Kaplan and Soodak'3 and Lennie andDerrington (personal communication) can accountfor the numerous types of threshold-suprathresholdrelationship that have been so far reported for nor-mal and anomalous vision. Following on from thisidea the present results suggest that, unlike amb-lyopia where the more sensitive contrast channelmay be selectively affected,'2 in optic neuritis allcontrast channels may be equally affected.

Optic neuritis thus represents a condition in whichno suprathreshold recruitment in contrast sensationoccurs; contrast thresholds and suprathreshold per-ception are equally affected. In this way the proces-sing of contrast by the visual system may have some-thing in common with the processing of loudness bythe auditory system. In audition, anomalies of theinner ear exhibit loudness recruitment. Analog-ously, the various amblyopias of vision exhibit con-trast recruitment. In audition, pathology to theauditory nerve does not result in loudness recruit-ment; thresholds and suprathreshold perceptionbeing equally affected or sometimes suprathresholdperception being more greatly affected.'4 In vision,the present results suggest that pathology to theoptic nerve results in analogous situation forcontrast (no recruitment).

I acknowledge the support obtained from the Medi-cal Research Council of Great Britain and the Well-come Trust. I am grateful to Clive Hood for techni-cal assistance and to Brian Moore, Gordon Plant,Jonathan Pointer, Robert Weale, David Tolhurstand Mark Georgeson for suggestions and usefuldiscussions. I am specially grateful to FergusCampbell for his encouragement and advice.



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References

Bodis-Wollner I. Visual acuity and contrast sensitivity inpatients with cerebral lesions. Science 1972;178:769-71.

2 Regan D, Silver R, Murray TJ. Visual acuity and con-

trast sensitivity in multiple sclerosis: hidden visualloss. Brain 1977;100:563.

3Zimmern RL, Campbell FW, Wilkinson IMSW. Subtledisturbances of vision after optic neuritis elicited bystudying contrast sensitivity. J Neurol NeurosurgPsychiatry 1979;42:407-12.

4 Georgeson M, Sullivan G. Contrast constancy: Deblur-ring in human vision by spatial frequency channels. JPhysiol (Lond) 1975;252:627-56.

s Kulikowski JJ. Effective contrast constancy. Vision Res1976;16:1419-31.

6 Hess RF, Bradley A, Piotrowski L. Contrast coding inamblyopia: I Differences in the neural basis of humanamblyopia. Proc Roy Soc B 1983;217:309-30.

7Sjostrand J, Abrahamsson M. Suprathreshold vision inacute optic neuritis. J Neurol Neurosurg Psychiatry1982;45:227-34.

Hess

8 Blakemore C, Campbell FW. On the existence ofneurones in the human visual system selectively sensi-tive to the orientation and size of retinal images. JPhysiol (Lond) 1969;203:237-60.

9 Watson AB, Pelli D. The Quest psychophysical proce-dure. Appl Vision Assoc Newsletter 1979;14:6-7.

10 Campbell FW. The eye as an optical filter. Proc IEEE1968;56:1009-14.

" Hess RF, Plant G. The effect of temporal frequency var-iation on contrast threshold deficits in optic neuritis. JNeurol Neurosurg Psychiatry 1983;46:322-30.

12 Hess RF. Contrast coding in amblyopia: II Physiologicalbasis of contrast recruitment. Proc Roy Soc B1983;217:331-40.

13 Shapley R, Kaplan E, Soodak R. Spatial summation andcontrast sensitivity of x and y cells in the lateralgeniculate nucleus of the macaque. Nature1981 ;292:543-5.

14 Dix MR, Hallpike CS, Hood JD. Observation upon theloudness recruitment phenomenon, with special refer-ence to the differential diagnosis of disorders of theinner ear and VIII nerve. Proc Roy Soc Med1948;41:516-26.



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