Use of displacement threshold hyperacuity to isolatethe neural component of senile vision loss

David B. Elliott, David Whitaker, and Penny Thompson

Displacement threshold hyperacuity is a visual task which should remain unaffected by the optical changeswithin the aging human eye. As such, it represents a method by which the neural component of senile visionloss may be studied. Displacement thresholds were measured in eighty subjects in the 18-85-yr age range.Results demonstrate a marked reduction in sensitivity with increasing age with the rate of deterioration beingproportional to the age of the subject. This can only be attributed to senile changes within the neural system.

1. Introduction

The rise in life expectancy has brought with it anobvious need to examine the physiological processesinvolved in aging. However, when considering studiesof the visual system, the interpretation of results ismade difficult because visual thresholds are depen-dent not only on underlying neural mechanisms butalso on the optical characteristics of the human eye.The effects of these factors need to be separated if anyfirm prediction is to be made regarding the extent ofsenile deterioration within the visual pathways.1

The optical factors associated with aging are welldocumented and can be considered under two catego-ries:

(1) Reduced retinal illumination. At a given levelof light adaptation the pupillary diameter decreaseswith age, a process known as senile miosis. Sinceretinal illumination is proportional to pupil area thesenile eye is required to operate at consistently lowerlevels of illumination. In addition, retinal illumina-tion will be further reduced due to increased lightabsorption by the lens which gradually opacifies withage. Therefore, when dealing with any visual thresh-old which exhibits a dependence on luminance, e.g.,visual acuity and contrast sensitivity,2 optical effectsmust be differentiated from neural ones. In severalstudies it has been concluded that retinal illuminanceplays a major role in spatial vision loss with age.3 -5

David Whitaker is with Aston University, Department of VisionSciences, Birmingham B4 7ET, U.K.; the other authors are withUniversity of Bradford, School of Optometry, Bradford BD7 1DP,U.K.

Received 31 May 1988.0003-6935/89/101914-05$02.00/0.3 1989 Optical Society of America.

(2) Increased light scatter. Inhomogeneities in re-fractive index which develop in the aging lens increaselight scatter and reduce contrast in the retinal image.Wolf and Gardiner6 have noted an increase in lenticu-lar light scatter with age, particularly in lenses over theage of forty. The significant acceleration in light scat-ter at this age is primarily due to the lens nucleus7 inwhich high molecular weight and water insoluble pro-teins accumulate.8 There is close agreement betweenthe age at which light scatter begins to increase and theage when visual function starts to decline. One study9

goes so far as to suggest that light scatter may accounttotally for the observed decline in contrast sensitivitywith age.

One way around the problem of distinguishing be-tween optical and neural age changes within the visualsystem is to use a stimulus which is unaffected by theoptical properties of the eye. An example of this islaser interferometry which produces interferencefringes on the retina without optical attenuation ordisturbance. Early studies using this technique foundno neural sensitivity loss with age,1011 although morerecent investigations have discovered a significant re-duction1213 and suggest that neural effects play themajor role in vision loss in the elderly. The evidence ofdeterioration in the aging visual system is considerableand includes retinal neurone loss, metabolic degenera-tion, lipofuscin accumulation, and cortical cell loss.14-17 The present study uses a similar idea to interferom-etry in that it involves a visual stimulus which is resis-tant to optical changes and, therefore, reflects the pro-cessing ability of the retina and neural system alone.The task represents a hyperacuity, that is, its thresh-olds are so small that they cannot be accounted for onthe basis of the spatial frequency content of the retinalimage. For example, although the optical media of thenormal human eye remove all spatial frequenciesabove -60 cycles/deg (corresponding to a peak to

1914 APPLIED OPTICS / Vol. 28, No. 10/ 15 May 1989

trough spacing of 30 sec of arc), hyperacuity thresholdsalmost an order of magnitude lower, than this are notunheard of.L18 In the same way as hyperacuities areunlimited by the optical aberrations and light scatterof the normal eye, so too are they resistant to bothartificial image degradation1 9 20 and degradation dueto disturbances within the optical media such as cata-ract.21 This has led to the clinical use of hyperacuitiesto evaluate visual function behind cataract.22-24

The hyperacuity task used in the present study wasthe oscillatory displacement threshold, defined as thesmallest amplitude of oscillation of a target, whichgives rise to the perception of movement. Thresholdsare highly dependent on both the temporal frequencyof the oscillation and the presence of nearby stationaryreferences against which displacement of the targetcan be judged.25 26 Thresholds for low temporal fre-quencies of oscillation (-2 Hz) can only be classed as ahyperacuity when stationary reference points areavailable. In their absence, no relative localizationjudgments can be made, and thresholds, therefore, fallwell outside the hyperacuity range. Since no position-al information is available in these conditions, thresh-olds presumably reflect the response of movement de-tecting mechanisms. However, when nearbyreferences are present, a precise location can be as-signed to the moving target at any time, and displace-ment thresholds of 10 sec of arc or less are common.The important point to note is that, if we wish to use astimulus which demonstrates maximum resistance toage changes within the media of the eye, we need toinclude stationary references to ensure hyperacuityperformance. At high temporal frequencies (above 10Hz) displacement thresholds show little dependenceon the presence of references. This is probably be-cause high frequency oscillations generate their ownreference since the subject is able to memorize targetlocation at one extremity of the oscillation cycle andcompare a subsequent positional change.

The rationale behind the present study, therefore,lies in the fact that displacement threshold hypera-cuity is unaffected by changes within the media of theeye. Its measurement in subjects of different ages,therefore, quantifies the deterioration in visual func-tion as a result of changes within the retina and neuralsystem alone.

II. Method

The target was projected onto a large translucentscreen via a small mirror. This mirror was mounted ona galvanometer system so that it could be made tooscillate about a vertical axis with simple harmonicmotion. In this way the target was made to oscillateback and forth, its amplitude and temporal frequencyof oscillation being controlled by a sweep functiongenerator. In all experiments the temporal frequencyof the oscillation was maintained at 2 Hz. The ampli-tude of the target oscillation was controlled by theexperimenter by means of a ten-turn variable potenti-ometer with a digital dial. The target was a vertical bar

of light 4 min of arc wide by 18 min of arc high with aluminance of 500 cd m-2. Two reference lines of iden-tical size and luminance were situated on either side ofthe target so that the edges of adjacent bars wereseparated by 60 min of arc.

Threshold amplitude of oscillation was determinedusing an ascending and descending method of limits.This method was chosen due to the likelihood of differ-ences in reaction time between age groups. The finalthreshold value was taken to be a mean of three as-cending and three descending estimates. Visual acu-ity measurements were made using the Logmarchart.27 This method has advantages over Snellenacuity in that there are the same number of letters oneach line, a regular progression of letter sizes, and eachline has an approximately equal difficulty of seeing.In addition, since the chart allows the measurement ofvery high acuity levels, it avoids the problem of trunca-tion of data to an arbitrary optimum level. Chartluminance was 160 cd m-2 and viewing distance 4 m.

Both oscillatory displacement thresholds and Log-mar visual acuity were measured in eighty patients inthe 18-85-yr age range. Most studies which have in-vestigated changes in visual function with age separatetheir results into two or three distinct age ranges andattempt to demonstrate that these groups differ statis-tically.28 The present study uses a different approachin that it uses a continuous age range of subjects, thusallowing the longitudinal effects of aging to be visual-ized. All subjects over the age of 50 yr were taken froma group who regularly underwent ophthalmoscopicand refractive examination at the University of Brad-ford. Exclusion criteria included previous eye disease,diabetes, intraocular pressure above 21 mm Hg, anylens opacity in the undilated pupillary area, and anyretinopathy. All subjects had normal maculas, de-fined as less than 4 drusen in an area of 1-disk diameteraround the macula and only slight pigmentarychanges. Younger subjects were either staff or stu-dents in the Department of Optometry and were ex-cluded from the study if they had any history of ambly-opia, squint, or eye disease. Each subject wasrefracted and wore their optimal correction for therelevant viewing distance when performing the tests.Thresholds were measured monocularly, only thedominant eye of each subject being investigated.

Although there is evidence of the resistance of dis-placement threshold hyperacuity to image degrada-tion and reduction in contrast (such as experienced bypatients with cataract),20 24 no previous study has in-vestigated the effect of luminance on oscillatory dis-placement thresholds in the presence of references.This clearly needs to be established if we are to at-tempt to separate neural aging effects from opticalones. For this reason a separate experiment was per-formed in which oscillatory displacement thresholdswere measured in a group of seven young subjects(mean age 24.3 ± 3.4 yr) with neutral density filters of0.7, 1.4, and 2.0 log units placed in front of their view-ing eye to reduce the luminance of the target andreferences.

15 May 1989 / Vol. 28, No. 10/ APPLIED OPTICS 1915

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Fig. 1. Displacement thresholds plotted as a function of age. Thebest fitting curve drawn through the data points is a second-order

polynomial with the equation y = 0.010x2 - 0.571x + 24.36.

111. Results

Figure 1 shows a scattergram of displacementthreshold as a function of age. It is clear that thresh-olds increase as a function of age, and this is confirmedby regression analysis (t7 = 9.12, p << 0.001). Allsignificance values are quoted on the basis of the nor-mal distribution of residual errors from the regressionanalysis. This was checked using the Durbin-Watsontest. A reasonable fit to the data can be achieved bylinear regression (r = 0.718), but a second-order poly-nomial produces a better correlation coefficient (r =0.793). The equation of the curve shown in Fig. 1 is

y = 0.010x 2 - 0.571x + 24.36.

Some previous investigations have divided their agerange into two groups, one comprising subjects belowthe age of 50 and another of 50 yr and above.29'30 If thesame is done for the present data, linear regressionreveals negligible slope for the younger age group (t31 =0.172, p = 0.865) and no significant correlation (r =0.031). The slope for the older age group is highlysignificant (t4 7 = 6.55, p << 0.001), and there is also asignificant correlation coefficient (r = 0.695).

With regard to visual acuity, Fig. 2 shows the rela-tionship between the minimum angle of resolution(obtained from the Logmar scores) and the age of thesubject. Again it is clear that thresholds increase as afunction of age (t 7 9 = 5.58, p << 0.001). Correlationcoefficients obtained from linear (r = 0.534) and sec-ond-order polynomial (r = 0.557) regression analysisare similar but less significant than for the displace-ment threshold data. The curve shown in the figurerepresents the best fitting second-order polynomialand has the equation

y = 0.005x2 - 0.188x + 42.59.

Dividing the data into young and old age groups, theslope of the linear regression fit to the younger group ismoderately significant (t3 = 2.21, p < 0.05) with aweak correlation coefficient (r = 0.374). The slope forthe older age group is highly significant (t47 = 3.69, p <0.001), and there is a weak to moderate correlation (r =0.477). The overall correlation between the minimum

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seven observers, standard errors being shown.

angle of resolution and displacement threshold wasalso weak to moderate (r = 0.473).

Figure 3 demonstrates the effect of luminance on theoscillatory displacement threshold. The initial lumi-nance of the target and references was 500 cd m-2, butthis was reduced using neutral density filters. Theresultant attenuation in luminance is plotted as theordinate. Analysis of variance of the data reveals ahighly significant effect of luminance (F3,1 8 = 14.8, p <<0.001), but multiple comparison analysis using theScheffe F-test revealed that this significance onlyarose due to the difference between the 2.0-log unitluminance level and the rest. None of the thresholddifferences between the other three luminance levelswas significant at the 90% confidence level.

IV. Discussion

The increase in oscillatory displacement thresholdswith age must be attributed to senile deteriorationwithin the neural system. It cannot be explained onthe basis of age changes in the optics of the eye, name-ly, reduced retinal illumination and increased lightscatter. The present results, shown in Fig. 3, demon-strate the independence of oscillatory displacementthresholds on luminance at all but very low levels. Asimilar weak dependence on luminance has been foundfor unidirectional target displacements.31 Compared

1916 APPLIED OPTICS / Vol. 28, No. 10/ 15 May 1989

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to the young eye, it has been estimated that the senileeye transmits -3 times (0.5 log units) less light onto theretina.3 2 Clearly, this will be expected to have a negli-gible effect on thresholds. With regard to the effect ofincreased light scatter, it has already been shown thatthis type of hyperacuity is highly resistant to degrada-tion of the retinal image.20 Whether the retinal imageis sharp or diffuse seems to make little difference toselected hyperacuity stimuli.19

It is easy to overemphasize the role of optical factorsin vision loss with age. Senile miosis and lenticularchanges actually enhance the retinal image in someways. The large pupil diameters of young adults leadto spherical aberration, but the average diameter of theaged pupil conforms quite well to the optimum.33

Chromatic aberration may also be reduced by senilelenticular changes which remove wavelengths at theextreme blue end of the spectrum.34 These factorsmay partially compensate for the loss of visual func-tion caused by increased light scatter and reducedretinal illuminance. Besides, the extent to which lightscatter affects visual function is questionable. Stud-ies investigating light backscatter from the lens haveshown that a surprisingly large amount of backscatteris necessary before a reduction in acuity is found. 7 8 Itis of interest to note that the effect of reducing illumi-nation serves to protect the older retina from poten-tially harmful radiation effects, especially in the, UVend of the spectrum. Furthermore, a self-limitingmechanism seems to be at work since exposure to UVlight produces chromophores, which are in themselvesa cause of increased lenticular absorption. 3 5

The increase in displacement thresholds with ageappears to follow a second-order polynomial function.This implies that the rate of deterioration within theneural system is proportional to the age of the subject.At a glance, this seems a reasonable suggestion. Itwould be somewhat more difficult to imagine a physio-logical system in which the rate of decline remainedconstant throughout life. Neurophysiological datatend to support the view of a gradual deterioration invisual function. Lipofuscin pigment in the retinalpigment epithelium increases gradually from 30 to 60yr and more rapidly in subsequent years.17 There isalso a gradual loss of cones and cone membranes be-tween 20 and 40 after which the rate of loss in-creases.1536 In addition to these retinal changes thereis an approximately linear reduction in neuron densityin the cortex between the ages of 20 and 87.18 Howev-er, it should be remembered that the rate of decline invisual function is not determined by neuron quantityalone but also by the functional quality of those cellswhich remain.1 7 18

The observed reduction in visual acuity with in-creasing age is consistent with previous findings.29'36

However, the level of acuity in the present data isbetter than found in previous studies. This can beattributed to two factors. First, our patients weresubject to strict criteria involving their ocular health,excluding those whose acuities were likely to be re-duced by some underlying pathology. Second, the use

of the Logmar chart tends to optimize acuity since itavoids the truncation effects which are inherent inmany visual acuity charts. There appears to be someincrease in data variability with increasing age in boththe acuity and displacement threshold data. Howev-er, this effect is fairly small and suggests that theclinical exclusion criteria used in the study successful-ly eliminated the majority of older subjects with ocularpathology.37 Although visual acuity has been shownto decrease with age, contrast sensitivity studies onaging have shown that, although sensitivity falls atintermediate and high spatial frequencies, it remainsunaffected at low frequencies. Low frequency con-trast sensitivity has been shown to play an importantrole in everyday visual activity3 8 and its retention withaging may be more advantageous than the fine detailafforded by high frequency channels.

A previous study also investigated the effect of agingon oscillatory displacement thresholds using ten sub-jects in each of three different age groups: 20-23, 40-55, and 60-80 yr.39 Displacement thresholds weremeasured for several oscillation frequencies rangingfrom 1 to 20 Hz. However, the stimulus was devoid ofstationary references, and this is reflected in thatthresholds fall outside the hyperacuity range. It is,therefore, unclear whether the observed increase inthresholds with aging was due to neural or opticaleffects, since low frequency unreferenced displace-ments have been shown to be affected by optical dis-turbance of the retinal image,20 and high frequencythresholds are badly affected by a reduction in con-trast.2 4

In addition to providing information regarding theneural component of senile vision loss, the presentresults also provide valuable normative data. The useof hyperacuities to assess visual function behind cata-ract has recently been advocated since such stimulihave the potential to distinguish between vision lossdue to the opacity and that which is due to retinal orneural dysfunction.222340 If oscillatory displacementthresholds are to play a part in this assessment, age-matched normative data are essential.

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1918 APPLIED OPTICS / Vol. 28, No. 10/ 15 May 1989