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427 Age dependence of saccades Correspondence and reprint requests to: Professor M. Fahle University of Bremen Human Neurobiology Centre for Cognitive Science Argonnenstr. 3 D 28211 Bremen Germany Tel: +49 421 218 9526 Fax: +49 421 218 9525 E-mail: [email protected] Acknowledgements: We would like to thank Prof. Dietz for advice regarding the statistical treatment of the data, Marc Repnow, Simon Bock, and Jakob Thiersch for generating computer code and hardware developments, Mrs. Weller for secretarial help, two anonymous reviewers for constructive criticism, and the Deutsche Forschungsgemein- schaft for financial support (SFB 517). Original paper Neuro-ophthalmology 0165- 8107/00/US$ 15.00 Neuro-ophthalmology – 2000, Vol. 24, No. 3, pp. 427-440 © Swets & Zeitlinger 2000 Accepted 21 November 2000 Age dependence of sensory and motor components in saccades M. Fahle 1,2 A.-J. Wegner 3 1 University of Bremen, Human Neurobiology, Centre for Cognitive Science, Bremen, and 2 City University London, Dept. of Optometry and Visual Science, London, UK 3 Universitäts-Augenklinik Tübingen, Sektion Visuelle Sensorik, Tübingen, Germany Abstract Humans usually perform about 3-4 saccades per second; hence, precision as well as latency and velocity of these fast eye move- ments are of crucial importance for analyzing complex and fast changing visual scenes, for example in traffic. Since visual performance is known to slowly decline with age, we investigated the effect of age on the most important characteristics of visually guided saccades. This inves- tigation on age dependence of visually guided saccades included, for the first time, the gap condition, where the old fixation point disappears before the new one appears, allowing subjects to prepare for a saccade. Saccadic latencies and intersaccadic intervals increased with age, while their peak velocities and gains decreased, especially for threshold-ad- justed luminance of the targets. The gap condition, however, improved reaction times (latencies) most pronounced in the older age groups, bringing performance for these groups close to the performance level of the young groups. This indicates that the slowing down of saccadic reaction times with age is not predominantly a motor problem, but, according to a common interpretation of the gap effect, a problem of disengaging attention from the old fixation spot. Key words Saccadic gain; saccadic reaction time; age dependence; eye movements; saccadic latency; saccadic precision; human Introduction The human visual system has an extremely steep gradient of resolution between the center of gaze, subserved by the fovea, and the periphery of the visual field. Hence, to analyze the visual world in detail, humans have to constantly scan the visual field by means of eye movements and they, on average, perform in the order of 10,000 saccades every hour during the day. The most important type of eye movements for this purpose are jumps to new positions or ob- jects – i.e. saccades. These saccades are very fast, quite precise, and have short latencies. Since resolution in the peripheral visual field is so poor, recognition of many objects requires precise foveation, and in Neuroophthalmology Downloaded from informahealthcare.com by Mcgill University on 11/13/14 For personal use only.

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Page 1: Age dependence of sensory and motor components in saccades

427Age dependence of saccades

Correspondence and reprintrequests to:Professor M. FahleUniversity of BremenHuman NeurobiologyCentre for Cognitive ScienceArgonnenstr. 3D 28211 BremenGermanyTel: +49 421 218 9526Fax: +49 421 218 9525E-mail: [email protected]

Acknowledgements:We would like to thank Prof. Dietz foradvice regarding the statisticaltreatment of the data, Marc Repnow,Simon Bock, and Jakob Thiersch forgenerating computer code andhardware developments, Mrs. Wellerfor secretarial help, two anonymousreviewers for constructive criticism,and the Deutsche Forschungsgemein-schaft for financial support (SFB 517).

Original paper

Neuro-ophthalmology 0165-8107/00/US$ 15.00

Neuro-ophthalmology – 2000, Vol. 24,No. 3, pp. 427-440© Swets & Zeitlinger 2000

Accepted 21 November 2000

Age dependence of sensory and motorcomponents in saccades

M. Fahle1,2

A.-J. Wegner3

1University of Bremen, Human Neurobiology, Centre forCognitive Science, Bremen, and 2City University London, Dept.

of Optometry and Visual Science, London, UK3Universitäts-Augenklinik Tübingen, Sektion Visuelle Sensorik,

Tübingen, Germany

Abstract Humans usually perform about 3-4 saccades per second;hence, precision as well as latency and velocity of these fast eye move-ments are of crucial importance for analyzing complex and fast changingvisual scenes, for example in traffic. Since visual performance is knownto slowly decline with age, we investigated the effect of age on themost important characteristics of visually guided saccades. This inves-tigation on age dependence of visually guided saccades included, forthe first time, the gap condition, where the old fixation point disappearsbefore the new one appears, allowing subjects to prepare for a saccade.Saccadic latencies and intersaccadic intervals increased with age, whiletheir peak velocities and gains decreased, especially for threshold-ad-justed luminance of the targets. The gap condition, however, improvedreaction times (latencies) most pronounced in the older age groups,bringing performance for these groups close to the performance levelof the young groups. This indicates that the slowing down of saccadicreaction times with age is not predominantly a motor problem, but,according to a common interpretation of the gap effect, a problem ofdisengaging attention from the old fixation spot.

Key words Saccadic gain; saccadic reaction time; age dependence;eye movements; saccadic latency; saccadic precision; human

Introduction The human visual system has an extremely steepgradient of resolution between the center of gaze, subserved by thefovea, and the periphery of the visual field. Hence, to analyze thevisual world in detail, humans have to constantly scan the visual fieldby means of eye movements and they, on average, perform in the orderof 10,000 saccades every hour during the day. The most important typeof eye movements for this purpose are jumps to new positions or ob-jects – i.e. saccades. These saccades are very fast, quite precise, andhave short latencies. Since resolution in the peripheral visual field is sopoor, recognition of many objects requires precise foveation, and in

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M. Fahle & A.-J. Wegner428

many instances, this foveation has to be achieved as fast and precise aspossible to identify possible dangers. To assess the ability to performfast and reliable saccades of different age groups whose members are(still) part of the production process, i.e., those most prone to dealingroutinely with complex and possibly dangerous visuomotor tasks, weinvestigated saccadic eye movements as a function of age.

Numerous studies1-11 have been published that address age-relatedchanges of the human sensory and motor systems. These studies indicate,among other things, that speed and precision of visually guided saccadesdecrease with age. However, it cannot be decided on the basis of thesestudies whether the decrease in performance is due primarily to motorfactors (so to speak, a slowing down of muscle power), sensory factors(for example, problems with detecting threshold-adjusted stimuli), ormore cognitive aspects such as shifts of attention and planning of theeye movements. (Of course, these three factors are not mutually exclu-sive, but may be superimposed). To disentangle the possible causes ofthe decay of performance with increasing age, we compared, using thesame observers, three experimental conditions. In the first condition,stimulus luminance and contrast of the saccadic targets were abovethreshold by about the same amount at every visual field position. Inthe second condition, contrast was far above threshold in order to eval-uate the influence of possible sensory (detection) problems, and in thethird condition, the so-called gap condition, the old fixation point disap-peared before the target appeared, giving the observers the opportunityto release attention from the old fixation spot and to prepare for saccadegeneration (cf. Fischer et al.,12 Reuter-Lorenz et al.,13,14 Reulen,15 Kleinet al.16). Disentangling these factors should lead us to a better under-standing of the effects of age on the different aspects of saccadegeneration, supply clinical norms for each aspect, and clarify thephysiological basis for possible compensating mechanisms. Our resultsindeed show that the temporal gap was long enough to allow even theolder observers to prepare well for the coming saccade generation,leading to a pronounced decrease in reaction times and results of theolder observers that were close to those of the young age groups underthis condition.

Material and methods

experimental setup Subjects were seated 60 cm in front of avertical opaque board with their head stabilized by a chin rest and browbar. The board contained LEDs which could be activated individuallyby a computer to serve as fixation targets (Fig. 1). The LED diameterwas 4 mm, corresponding to 23 arcmin, i.e. roughly the second-largesttest size in Goldmann perimetry. Horizontal and vertical eye move-ments were recorded by an infrared eye tracker (AMTech) with a tem-poral resolution of 240 Hz and a (theoretical) spatial resolution of 0.5arcmin. The distance between neighboring LEDs was 5°; they spanned60° (±30°) horizontally for all observers and 20° (±10°) vertically forsome and only 10° for others due to limitations of the eye tracker.Observers were asked to change their gaze towards a new target LEDupon its illumination. After the saccade, that target LED became the

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429Age dependence of saccades

Fig. 1. Schematic drawing of theboard containing the array of targetLEDs. The LEDs were arranged atdistances of 5° from each other alongboth the horizontal and verticalmeridian. Maximum distance from themiddle was 30° horizontally and 10°vertically. The apparatus allowedregistration of the 20° up and downsaccades in most, but not all observers.

new fixation point. The order of testing of the saccades was pseudo-random, and the presentation time of each LED lasted between 1 and2 s. LEDs were flickered at a frequency of 90 Hz, their luminance wasvaried by adjusting the pulse width (or duty cycle) of the flicker im-pulses. Background luminance was constant at 6 cd/m2.

subjects Forty subjects aged between 22 and 69 years participatedin this study. They were divided into four age groups comprising 10subjects each. Group 1 consisted of five women and five men agedbetween 22 and 30 years. Group 2 included five women and five menaged between 31 and 45 years, while group 3, aged between 46 and 60years, consisted of eight women and two men. The oldest group (group4) was formed by seven women and three men in their sixties. Visualacuity of all observers was at or above 0.8 (15/20) and none of theobservers suffered from a history of eye disease or neurological disor-der. Observers wore their normal optical corrections if any.

experimental conditions Each subject took part in three differ-ent tests. For the first test, threshold-adjusted luminance, LED lumi-nance depended on the eccentricity of the target and was about a factor5 above threshold for each eccentricity, as determined in a pilot study.This adjustment followed the graduation in the visual field used inmodern automated perimeters such as the Tübinger Automatic Perim-eter presenting stimuli at contrasts that are about equally far above thenormal threshold for each visual field position (see, e.g., Aulhorn17).Under this condition, the targets were subjectively easily detected byall observers at all eccentricities. Target-LED luminance ranged be-tween 6.7 cd/m2 for saccades of 5° amplitude and 33 cd/m2 for saccadesof 60° amplitude on a background of around 6 cd/m2. Under the secondcondition, LED luminance was constant at 50 cd/m2 at all eccentrici-ties. In these two conditions, the old fixation point disappeared at thetime of appearance of the new fixation point in order to clearly indicatethe time of appearance even for threshold-adjusted stimuli. Hence,observers were always aware of when to generate a saccade, unlike thecase of an overlap condition of the old and new stimulus when the newstimulus may not be clearly detected. For the third condition, there wasa temporal gap of 200 ms between the extinction of the fixation LEDand the presentation of the target LED. Luminance was again constantat 50 cd/m2. Altogether, each subject contributed about 70 primary

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M. Fahle & A.-J. Wegner430

saccades, i.e., first saccades towards the target in each of the threeconditions, resulting in a data pool of around 8400 saccades for thisstudy.

analysis of eye movements Saccades were classified off-line.Criteria for the identification of saccades were a minimal starting ve-locity of 10°/s and a minimal mean velocity of 40°/s. Saccades wereclassified as primary saccades (correct direction, saccadic reaction timebetween 100 ms and 1 s), secondary or correction saccades, searchsaccades (wrong direction and/or saccadic reaction time above 1 s), andanticipatory saccades (saccadic reaction time shorter than 100 ms). Weused this rather conservative limit for anticipatory saccades rather thanthe 80 or 85 ms used in Wenban-Smith and Findlay18 to accommodatethe fact that some of our observers were older than those in most otherstudies. This value is still below the latency of most express saccades,which occur at a mean latency of about 95-115 ms (see Fischer &Ramsperger19) or between 100 and 135 ms (as in Fischer et al.12) andbelow the 120 ms suggested by Kalesnykas and Hallet20 for the timeinterval between saccades. As Figure 5 shows, the exact choice of limithas only very little impact on the results.

We measured (a) gain of the primary saccades as a function of therequired jump size, (b) reaction time of the primary saccades (latency;ms), (c) peak velocity of the primary saccades (°/s), (d) intersaccadicinterval (ISI) between primary saccades and correction (i.e. secondary)saccades (ms), and (e) distribution of different types of saccades (4types). For analysis, the gain and the ISI were log10-transformed andthe reciprocal of the saccadic reaction times was used21 since the reci-procals were normally distributed, while the reaction times were not,and a normal distribution is a prerequisite for most statistical tests.

The main sequence, i.e. the relationship between amplitude and peakvelocity, was fitted with the exponential function f(x)=a-a*e(-x/c), wherea is the asymptotic velocity reached for large saccadic amplitudes andc is a constant. With the transformed gain, ISI, saccadic reaction times,and the parameter a (asymptotic peak velocity), an ANOVA with factors‘age’, ‘condition’, ‘hemifield’, and ‘jump size’ was calculated.

Results

gain of saccades The relative amplitudes of saccades, expressedas the gain (i.e., the percentage of required amplitude actually coveredby the primary saccade) depends on the absolute distance between theold and the new target of fixation. The larger the required jump sizebetween these targets, the smaller the gain usually is. This findingholds true for all age groups. Figure 2a shows the gain separately forall age groups as a function of jump size, together with regressionsthrough the data for stimuli of threshold-adjusted luminance contrast.The ANOVA detected significant influences on gain by age (p=0.05),visual hemifield (p<0.001), condition (p<0.001), jump size (p<0.0001),age*condition (p<0.05), and age*jump size (p<0.0001). We did notfind significant sex differences in any of the results.

Gain decreased more in the left than in the right hemifield, and more

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Page 5: Age dependence of sensory and motor components in saccades

431Age dependence of saccades

Fig. 2. (a) Gain of primary saccades asa function of required jump size for allfour age groups. Group 1: ages 22-30;group 2: ages 31-45; group 3: ages 46-60; group 4: ages 61-69 years. Linesindicate linear regressions through thedata; the corresponding formulae areindicated. Results of 10 observers ineach age group for threshold-adjustedluminance. Data are collapsed, foreach observer, over all polar angles ofsaccade direction. (b) Slope ofregression lines through the data ongain as a function of required jumpsize for all age groups and all threeconditions tested (Data from Fig. 2aare replotted via their slopes andindicated by squares). Decrease ofgain with increasing jump size is mostpronounced for the threshold-adjustedluminance condition (steeper negativeslopes), and most pronounced for theoldest age group.

2a

2b

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for wider jump sizes. The decrease with jump size was most pronouncedin the threshold-adjusted luminance condition and for the oldest agegroup (see Fig. 2a), less in the gap, and least in the constant luminancecondition (p<0.001). The slopes of regression lines through the dataexemplified in Figure 2a for the threshold-adjusted condition are shownin Figure 2b for all experimental conditions in all observers. Althoughthe decrease of gain with required jump size becomes steeper withincreasing age for all conditions, it is most pronounced for the threshold-adjusted condition (squares in Fig. 2b).

latency (reaction time) of saccades The latency of saccadeswas similar for all jump directions (Fig. 3), but was longer for largersaccades than for shorter ones (p<0.001) as seen in Figure 4 for thethreshold-adjusted luminance condition. The other conditions yieldedsimilar results.

Distribution of reaction times depended on age group and on condition,with anticipatory saccades being relatively frequent in the gap condition(Fig. 5). Latencies, as all reaction times, tend not to be normally dis-tributed. Therefore, we used the median latencies of every observer,separated according to conditions, rather than the means. For this anal-ysis, anticipatory saccades, i.e., those below 100 ms, were discarded, asoutlined in the Methods section. These data were used to calculate thedependence of latencies on age under the three presentation conditions.

Latencies were longest with the threshold-adjusted luminance, mediumfor the constant luminance, no gap condition, and shortest for the gapcondition (p<0.001). Latencies for all conditions increased with age(p<0.001) The increase was four times more pronounced for the thresh-old-adjusted luminance condition (slope=2.39; p<0.001) than for theconstant condition (slope=1.317) and the gap condition (slope=0.59;p<0.01 for interaction age*condition; cf. Fig. 6). The rather shallow

Fig. 3. Latency of primary saccades asa function of jump direction (polarangle). Results for the constantluminance condition, averaged overall observers of all age groups.Numbers on the circumference of thelargest circle indicate the direction ofsaccades. The distance between thecenter of the circle and the data pointsindicates the latency: each (additional)circle represents an additional 50 ms.

Fig. 4. Latency of primary saccades asa function of required jump size,averaged over all observers of all agegroups, for the adjusted luminancecondition.

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433Age dependence of saccades

Fig. 5. Distribution of latencies (a) forage group 1 under the constantluminance condition, (b) for age group1 under the gap condition, (c) for agegroup 4 under the constant luminancecondition, and (d) for age group 4under the gap condition.

increase of latencies with age under the gap condition means that olderobservers benefit strongest from the temporal gap and that their resultsin the gap condition differ only slightly from those of the youngest agegroup.

peak velocity of primary saccades The maximal velocity ofprimary saccades decreased with age (Fig. 7), with the difference be-tween the youngest (group 1) and oldest age groups being highly sig-nificant (p<0.001). Regressions through the data on peak velocity as afunction of age yielded slopes of -1.59 (gap condition), -1.84 (adjustedcondition; Fig. 7), and -1.85 (constant luminance condition), all signif-icantly different from zero. Maximal velocity was highest for constantluminance and lowest for the gap condition (p=0.02), and faster to theright than to the left (p<0.0001).

intersaccadic interval Similar to the latencies, the length of theintersaccadic intervals was not normally distributed. Therefore, the log10-transformed values were used for analyses. The intersaccadic intervalsdepended on the stimulus condition, with the shortest intervals obtainedin the gap condition and the longest intervals in the threshold-adjustedluminance condition (p=0.0028). Intersaccadic intervals for all condi-tions increased with age (p=0.001, Fig. 8) as well as with jump size

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Fig. 6. Influence of age on saccadiclatencies. Medians of individuallatencies for all observers of thedifferent age groups under all threeconditions. (a) adjusted luminance; (b)constant luminance; (c) gap condition.

Fig. 7. Maximal velocity of primarysaccades as a function of age. Resultsof all observers of all age groups, forthe adjusted luminance condition,expressed as the factor ‘a’ of theregression through the individual dataof each observer in a plot of velocityas a function of jump size (f(x)=a-a*e(-x/c)).

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(p=0.0033). The interaction between age and condition is significant(p=0.0097), as is the influence of hemifield (p<0.0001), with longerISIs to the right. This increase of intersaccadic interval complementsthe decrease of gain with increasing age.

distribution of saccadic types As mentioned in the Materialand Methods section, we discriminate between primary, secondary, an-ticipatory, and search saccades. The distribution of these different typesof saccades for the threshold-adjusted luminance and the gap conditionis shown in Figure 9 for all age groups. Primary and secondary sac-cades are most frequent, especially in the younger subjects, while thereis a large proportion of search saccades in the higher age groups.

Discussion

gain of saccades as function of amplitude For all age groups,larger required saccadic jump sizes led to a more pronounced under-shoot, i.e., smaller gain, than smaller jump sizes under the threshold-adjusted luminance and gap conditions. Please note that the gain indi-

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435Age dependence of saccades

Fig. 8. Intersaccadic intervals as afunction of age. Medians of allobservers for the three stimulusconditions averaged over jump sizes.

cates the relative size of the saccades – hence, the undershoot increaseswith jump size more than in proportion; not only the absolute, but alsothe relative error increases with jump size. This result is consistent withthe findings of Frost and Pöppel,22 Zambarbieri et al.,23 and Sharpe andZackon,24 but not with the data published by Lemij and Collewijn.25

These latter researchers found an increase of absolute, but not of relativeerror with increasing jump size. Quite to the contrary, their relativeerrors decreased with increasing jump size. Our observers yielded muchhigher gains than those of Lemij and Collewijn, namely between 95%and 106% (depending on stimulus condition) for the 10°-wide saccades,while observers in the earlier studies yielded gains around 85%. For the40°-wide saccades, our observers yielded gains between 86% and 97%under the constant luminance condition and between 79% and 94%,depending on age group, under the gap condition. Those of the Lemijand Colewijn group obtained comparable gains around 90% for thisjump size.

The most probable reason for the difference between the two types ofresults is the fact that in the Lemij and Collewijn study, observers knew

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in advance when and where the next fixation point would appear. Thiswas not the case in our study. Knowledge about the next fixation pointis expected to increase the percentage of anticipatory saccades and thuslead to smaller gains than for visually guided saccades.

Some studies did not find any correlation between the amplitudes ofsaccades and gain.26,27 These studies did not, however, indicate theluminance of the stimuli used. The most probable design would beclearly suprathreshold stimuli such as in our constant luminance con-dition. In this condition, our observers also demonstrated a smallerdependence of gain from jump amplitude than in the threshold-adjustedcondition. So, in summary, it seems fair to conclude that gain indeeddecreases with jump size, especially for threshold-adjusted stimuli andin the oldest age group (cf. Fig. 2b).

gain of saccades as a function of age The average gain ofsaccades decreases with age. This result is in agreement with the find-ings by Sharpe and Zackon,24 who report that frequency of hypometricsaccades increases with age (cf., however, Warabi et al.26). Gain de-creases with required jump size far more pronounced in the oldest agegroup than in the other age groups, strongest in the adjusted luminancecondition, clearly less so in the gap condition, and least in the constantluminance condition (Fig. 2b).

Decrease of gain with jump size is most pronounced under the thresh-

Fig. 9. Distribution of different typesof saccades in percent under the (a)adjusted luminance and (b) gapcondition, separately for the four agegroups.

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437Age dependence of saccades

old-adjusted luminance condition in all age groups, leading to the steep-est negative slopes in Figure 2b. Several factors may contribute to thiseffect, such as the longer perceptual latencies for peripheral stimuli.However, it is surprising that the decrease of gain with jump size ismore pronounced under the threshold-adjusted condition, since thiscondition should at least partly compensate for the reduced sensitivityof the peripheral retina. A possible explanation is that the gain isrelatively independent of luminance for clearly suprathreshold stimuli,but that peripheral targets are not sufficiently above threshold (max.luminance of 33 cd/m2) for 60° saccades under the adjusted luminancecondition, while the constant luminance condition employs a quite highluminance throughout (50 cd/m2).

latency of saccades Latency of primary saccades increases sig-nificantly with increasing amplitude (Fig. 4). Hence, we confirm theresults of Kalesnykas and Hallett,20 who found a significant relation,while our results disagree with those of Frost et al.,22 Zambarbieri etal.,23 and Wilson et al.28

Under all conditions, older subjects required significantly longer la-tencies of primary saccades than younger age groups (Fig. 6), well inline with the results of Spooner et al.,29 Abel et al.,30 Warabi et al.,26

Sharpe and Zackon,24 and Wilson et al.28 Latencies were longest underthe threshold-adjusted condition, shorter under the constant luminancecondition, and shortest under the gap condition (that employs constantluminance), indicating an influence of target luminance on saccadelatency, as found by Boch et al.31 and Kalesnykas and Hallett.20 Thus,this is a clear demonstration that sensory processes play a significantrole in saccadic latencies: as to be expected, threshold-adjusted contrastsled to an increased latency that can be ascribed to increased detectiontimes for the stimulus.

The temporal gap between extinction of the fixation point and pre-sentation of the target also had a distinct influence on latency, firstdescribed by Saslow32 and extensively further investigated by Fischerand co-workers (see, e.g., Ref. 33). This shortening of latencies, thegap effect, is ascribed by some authors such as Fischer to the fact thatduring the gap, attention can be disengaged from the fixation point andtherefore be moved faster to the new saccadic target.

The gap effect increased with age, ranging from about 22 msec in theyoungest age group to about 50 msec in the oldest subjects (Fig. 6).Hence, the oldest age group benefited more than twice as much fromthe temporal gap than the younger age groups did, approaching, for thegap condition, the results of the younger groups. Since the motor taskis identical under both conditions, as is the spatial configuration (andall possible undetected eye diseases in our observers), the purely motorpart of saccade generation cannot be causing the decrease of latencies.Thus, our results indicate that the increase of saccadic reaction timeswith age is not predominately a motor problem – nor is it a purelysensory problem. The only difference between the two conditions liesin the time of stimulus appearance allowing observers to start with-drawing attention from the old fixation point and getting ready to cal-culate a saccade. Obviously, older observers have more problems, or

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require more time, with this aspect of saccade generation, since theybenefit so much from the gap condition. We would like to stress againthe fact that this effect cannot be caused by possible eye diseases thatare more prevalent in older age groups.

This increased benefit of cueing – if we consider the temporal gap asa kind of temporal cue – in the older age group differs from the effectof cueing of attention in visual tasks. Wright et al.34 investigated theeffect of pre-cueing attention to one or the other visual hemifield. Theyfound a decreased response time benefit of cueing in their older thanin their younger age groups. Similar results have been described for thecueing of attention in a visual search task: again, the benefit of pre-cues decreased with age.35 The motion of attention to a cued locationwas slower in older than in younger observers, and more easily dis-turbed by nontarget stimuli in the older group of observers.36 Thesedifferences between the results on moving an ‘attentional spotlight’ toa position in space versus getting ready to move the eyes to a newposition reflect important differences between the two types of cueing.In the conventional cueing tasks, observers not only disengage attentionfrom the previous location, but also move it to a new location. Thisability seems to slow down with increasing age. However, if one acceptsthat the gap effect is indeed due to a disengagement of attention fromthe old location, then the duration of the gap is obviously long enoughfor all age groups to disengage attention. Our results, therefore, indicatethat the difference between the age groups is primarily due to a slowerdisengagement of attention in older age groups. Under the conditionsof the gap effect, this difference is compensated for by a sufficientduration of the gap; hence, the differences between age groups arereduced to differences in the ability to plan and perform a saccade toa new position – and these differences seem to be rather small. Clearly,more experiments are required to test this hypothesis, for example byusing shorter gap durations.

velocity of saccades The peak velocity of saccades decreasessignificantly with age in spite of large inter-individual differences (Fig.7; compare also References 24, 26, 29 with 30, 37). Also, the factorcondition has a significant influence on peak velocity: the gap condi-tion leads to the lowest velocities, the constant luminance condition tothe highest velocities. The results for the threshold-adjusted conditionare not significantly different from the other two conditions. So, wefind that there may be a partial trade-off between latency and velocityof saccades: saccades with a short latency do not reach highest veloc-ities.

intersaccadic interval and distribution of saccade typesUnder all three conditions, the intersaccadic interval (ISI) increasedsignificantly with age, i.e., older subjects needed a significantly longertime to correct the positional error present after the end of the primarysaccade (Fig. 8). Since the gain of older subjects is smaller, too, thepositional error in these subjects is larger than in the younger subjectsand they have to produce larger corrective saccades than the youngerobservers. Our results indicate that older subjects require a longer time

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439Age dependence of saccades

interval to produce these larger secondary (correcting) saccades. Ac-cording to Becker,38 larger positional errors should lead to shorter ISIs.This is not what we found here. A possible explanation is that the ageeffect is so strong that it masks the (smaller) effect of spatial error size.ISIs are, on average, 11 msec shorter under the constant than under thethreshold-adjusted luminance condition. Surprisingly, the gap conditionleads to the shortest ISIs – as if the disengagement of attention couldalso transfer to the secondary saccade. A possible explanation could bethat both primary and secondary saccades were planned as a whole andtherefore many of the secondary saccades are not visually guided, i.e.not caused by visual error feedback.

Under the threshold-adjusted luminance condition, we found a largerproportion of ‘search’ saccades, especially in the oldest group, indicatingthat the subjects did not immediately perceive the targets. The gapcondition, as to be expected, provided the highest proportion of shortlatency primary saccades.

conclusions By varying stimulus luminance and the timing ofstimulus presentation, we were able to partly discriminate betweenmotor, sensory, and (possibly) cognitive factors in the increase of sac-cadic latency with increasing age. The disappearance of the old fixationpoint before the presentation of the saccadic target in the gap conditionimproved reaction times in older observers more than twice as much asin younger observers, almost levelling off the age differences in laten-cies. This result cannot be caused by possible eye diseases in the olderage groups and indicates that the increase in saccadic latencies withincreasing age is mostly due to attentional and cognitive factors. More-over, our results indicate that the cueing of stimuli, for example ineveryday situations, should improve saccadic reaction times in olderobservers.

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