Vision Research 46 (2006) 2581–2592www.elsevier.com/locate/visres

Characteristics of accommodative behavior during sustained reading in emmetropes and myopes �

Elise Harb ¤, Frank Thorn, David Troilo

The New England College of Optometry, 424 Beacon Street, Boston, MA 02115, USA

Received 8 October 2005; received in revised form 1 February 2006

Abstract

Accommodation has long been suspected to be involved in the development of myopia because near work, particularly reading, isknown to be a risk factor. In this study, we measured several dynamic characteristics of accommodative behavior during extended periodsof reading under close-to-natural conditions in 20 young emmetropic and stable myopic subjects. Accommodative responses, errors, andvariability (including power spectrum analysis) were analyzed and related to accommodative demand and subject refractive error. Allaccommodative behaviors showed large inter-subject variability at all of the reading demands. Accommodative lags and variability sig-niWcantly increased with closer demands for all subjects (ANOVA, p < 0.05). Myopes had signiWcantly greater variability in their accom-modation responses compared to emmetropes (ANOVA, p < 0.05) and had larger accommodative lags at further reading distances(unpaired t test p < 0.05). Power spectrum analysis showed a signiWcant increase in the power of accommodative microXuctuations withcloser demands (ANOVA, p < 0.05) and with increasing myopia at the closest reading demand (ANOVA, p < 0.01). The diVerence in thestability of the accommodative behavior between individuals with diVerent refractive states suggests a possible relationship between vari-ability in accommodation and the development of myopia.© 2006 Elsevier Ltd. All rights reserved.

Keywords: Accommodation; Myopia; Reading; Accommodative microXuctuations

1. Introduction

A correlation between myopia and education (e.g., Al-Bdour, Odat, & Tahat, 2001; Au Eong, Tay, & Lim, 1993;Hepsen, Evereklioglu, & Bayramlar, 2001; Richler & Bear,1980; Young et al., 1969) is well known and has led to specu-lation that the amount of reading a child does may be a riskfactor for the development of myopia. Additional research hassuggested that accommodation is the link between near workand myopia (reviewed by RosenWeld, 1998; RosenWeld & Gil-martin, 1998b) but there is little direct evidence for or againstthis assertion. Several aspects of accommodation have beensuggested as possible risk factors; decreased accommodativetonus (McBrien & Millodot, 1987; RosenWeld & Gilmartin,

� Supported by NIH R01 EY11228 (D.T.) and T35 EY07149 (E.H.).* Corresponding author. Fax: +1 6172366325.

E-mail address: harbe@neco.edu (E. Harb).

0042-6989/$ - see front matter © 2006 Elsevier Ltd. All rights reserved.doi:10.1016/j.visres.2006.02.006

1987), decreased accommodative amplitude (McBrien &Millodot, 1986), increased accommodative lags (Abbott, Sch-mid, & Strang, 1998; Gwiazda, Thorn, Bauer, & Held, 1993;Gwiazda, Thorn, & Held, 2005; Nakatsuka, Hasebe, Nonaka,& Ohtsuki, 2005), increased accommodative adaptation(Chen, Schmid, Brown, & Edwards, 2005; Culhane & Winn,1999; Gilmartin & Bullimore, 1991; Gwiazda, Bauer, Thorn,& Held, 1995b; McBrien & Millodot, 1988; Strang, Winn, &Gilmartin, 1994), and increased accommodative Xuctuations(Day, Strang, Seidel, Gray, & Mallen, 2006; Seidel, Gray, &Heron, 2003) have all been shown in myopes, although it isunclear how such risk factors might induce myopia.

Hyperopic retinal defocus resulting from a large accom-modative lag during periods of extended near work mightresult in compensatory axial elongation of the eye andmyopia (Abbott et al., 1998; Gwiazda, Bauer, Thorn, &Held, 1995a; Gwiazda et al., 1993; Gwiazda et al., 2005;Nakatsuka et al., 2005). Animal studies have shown that

2582 E. Harb et al. / Vision Research 46 (2006) 2581–2592

imposing hyperopic defocus with negative lenses induces acompensatory increase in eye growth and myopia (Graham& Judge, 1999; Hung, Crawford, & Smith, 1995; SchaeVel,Glasser, & Howland, 1988; Whatham & Judge, 2001).These studies, together with compensatory axial hyperopiaseen in response to positive lenses (SchaeVel et al., 1988;Smith, Hung, & Harwerth, 1994; Whatham & Judge, 2001),provide strong evidence that eye growth and refractivedevelopment are visually guided (see Wallman & Winawer,2004 for a recent review).

Variability in the accommodative response to near tar-gets over sustained periods of time as in reading has notbeen described, but may be related to myopia in a numberof ways: (1) Xuctuations in retinal defocus associated withaccommodative variability may be a risk factor for thedevelopment of myopia (Plainis, Ginis, & Pallikaris, 2005).Even if the mean accommodative responses show little lag,increased accommodative variability that increases hyper-opic retinal defocus during near viewing could be inte-grated over time and lead to myopic shifts (Wallman &Winawer, 2004). (2) Accommodative variability may reXectthe sensitivity of accommodation to hyperopic blur, andlow blur sensitivity may be a risk factor for the develop-ment of myopia. Myopes have been reported to havereduced sensitivity to retinal blur (Jiang, 1997; RosenWeld& Abraham-Cohen, 1999), which would result in largeraccommodative lags because a larger amount of hyperopicblur would be required to elicit an accommodative responseand this could cause accommodation to oscillate duringnear viewing over a wider-than-normal range (Day et al.,2006; Seidel et al., 2003). (3) The elongation of the myopiceye may aVect the shape of the anterior segment, whichcould theoretically increase variability in the accommoda-tive response. Mutti, Jones, Moeschberger, and Zadnik(2000) hypothesized that increased mechanical tension onthe ciliary body in the elongated eyes of myopes createsgreater hyperopic lags (termed “pseudo-cycloplegia”), andaccommodation has been suggested to aVect eye shape aswell (Walker & Mutti, 2002).

Studies of accommodation in humans are typically per-formed during brief near tasks under tightly controlledenvironments in order to understand the stimuli drivingaccommodation and the dynamics of the accommodativeresponse (e.g., Alpern & David, 1958; Campbell & Westhei-mer, 1960; Fincham, 1951; Heath, 1956; Kruger, 1980; Kru-ger & Pola, 1989; Phillips & Stark, 1977). However, verylittle is known about accommodative behavior during sus-tained periods of reading in natural visual environments. Inthis study we concentrate our attention on the variability ofthe accommodative response. Understanding how individu-als vary in their accommodative behavior and their abilityto sustain focus on the plane of text while reading is impor-tant for understanding any relationship between accommo-dation, near work, and the development of myopia(SchaeVel, Weiss, & Seidel, 1999). The aim of this study is toidentify and describe several aspects of accommodativebehavior over sustained periods of reading in a close-to-

natural setting and to determine whether diVerences inemmetropes and myopes exist. Preliminary reports of thisstudy have been presented in abstract form (Harb, Thorn,& Troilo, 2003; Harb, Thorn, & Troilo, 2004).

2. Methods

2.1. Subjects

All research performed in this study adhered to the tenets of the Decla-ration of Helsinki and was approved by the Institutional Review Board ofThe New England College of Optometry. All subjects who participated inthis study also provided written informed consent. Accommodation dur-ing reading was examined in 20 subjects (optometry students aged 22–28years) with normal binocular vision, stable spherical equivalent refractiveerrors ranging from +0.50 to ¡7.0 D (11 myopes and 9 emmetropes), andless than ¡0.75 D of astigmatism. Emmetropia was deWned as +0.50 to¡0.50 D. Stability of refractive error was self-reported by the subjects anddeWned as a change of §0.50 D over the last two years. During testingmyopic subjects were fully corrected with their contact lens corrections.

2.2. Reading task

Subjects read an excerpt from a novel (black letters on a white back-ground—Times New Roman font) displayed on a computer monitor atthree diVerent distances (66.6, 40, and 28.6 cm) corresponding to accom-modative demands of 1.5, 2.5, and 3.5 D. The accommodative response toa visual display terminal does not diVer from printed text (Sorkin, Reich,& Pizzimenti, 2003), therefore, a computer monitor was used to allow forgreater control over stimulus presentation. The actual size of a text win-dow placed on the visual display terminal was modiWed to allow for a con-served angular subtense of 9.5° horizontal£ 4.5° vertical at all readingdistances. Letter height was also maintained at an angular subtense of0.36° for all distances. On average the luminance of the visual display ter-minal was 14.3 c/m2 during the reading task. Subjects were instructed toread silently for 10 min. The subjects were able to control their own read-ing pace by scrolling within the text window. Subjects were instructed toread as they would normally and were allowed to look away from the textat their discretion while maintaining their head in the chin-rest. The num-ber of Wxation breaks was recorded. Although the subjects were not testedfor reading speed or comprehension of the reading material, appropriatesaccadic eye movements consistent with reading were observed by theexaminer (E.H.) throughout the task. Reading tasks at all three workingdistances were performed in a random order within a single day.

2.3. Measurement of accommodation and eye position

Refractive state, pupil diameter, and eye position were measured bin-ocularly (only one eye used for accommodation analysis) at a rate of 25 Hzusing an eccentric infrared photorefractor (PowerRefractor–MultiChan-nel Systems; Reutlingen, Germany). For continuous recording, the Pow-erRefractor measures refractive state in the vertical meridian. ThePowerRefractor was positioned 1 M away from the subject, 5°–8° abovethe text window, and was directed between the subject’s eyes. The infraredlight source has been established for safe use with adults and children(Choi et al., 2000).

The pupils of all subjects were dilated with two drops of 2.5% phenyl-ephrine 45 min prior to measurements to prevent signiWcant changes inpupil size. Although this is not considered a natural state for reading,subject’s pupils were dilated to reduce Xuctuations in pupil size thatcould aVect the performance of the optometer. The PowerRefractor hasbeen shown to have no systematic change in refraction measures withvarying pupil sizes (Choi et al., 2000) within a narrow range of relativelylarge pupil sizes (approximately 4–7 mm), but the accommodativedemands in our set-up often resulted in pupil constriction outside of thisreliable range. Phenylephrine has been reported to result in a small

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reduction in accommodative amplitude (11%) (Culhane, Winn, & Gil-martin, 1999; Gimpel, Doughty, & Lyle, 1994), but others found nointerference with the accommodative response (CiuVreda, 1998), includ-ing the dynamics of the response (Ostrin & Glasser, 2004). If present, thesmall decrease in the amplitude of accommodation associated withphenylephrine administration in young subjects with large amplitudes ofaccommodation (Hofstetter’s minimum amplitude D 9.5 D for a 22-year-old and 8.0 D for a 28-year-old, (Hofstetter, GriYn, Berman, & Everson,2000)) would not aVect accommodative responses at normal reading dis-tances. Although not speciWcally measured, it is plausible that theincreased pupil sizes will increase the inXuence of aberrations on theaccommodation measurements made by the PowerRefractor. Because ofthe arrangement of the LEDs, the PowerRefractor is less aVected byasymmetric aberrations compared to photorefractors with a singlesource design (Roorda, Campbell, & Bobier, 1995). The eVect of spheri-cal aberrations, however, will theoretically be averaged into the readingsand bias the measured refractions by small (<0.2 D) amounts. Althoughthe eVects of spherical aberrations on the operation of the PowerRefrac-tor has not been empirically tested at this time, it has been shown inautorefractors that positive spherical aberration biases toward myopiaand negative spherical aberration biases toward hyperopia (Hazel, Cox,& Strang, 2003; and reviewed by Charman, 2005).

2.4. Calibration of the PowerRefractor

The PowerRefractor was calibrated with a separate group of 21 sub-jects (21–28 years of age) with normal binocular vision and refractiveerrors ranging from +1.00 to ¡5.00 D (spherical equivalents). This range iswithin the limits of the PowerRefractor (§5 D) as described by Choi et al.(2000). Subjects were cyclopleged with two drops of 1.0% cyclopentolate45 min prior to calibration measurements to control for pupil size andaccommodation. Some subjects (n D 12) were measured both while uncor-rected and while wearing their contact lens corrections in order to increasethe range of refractions measured.

After cycloplegia, retinoscopy and subjective refraction measures wereperformed by two separate experienced examiners (E.H. and F.T.) andwere signiWcantly correlated (R D 0.94, p < 0.01). In the same subjects,PowerRefractor measures were made in the vertical meridian while thesubject looked at a high contrast 20/100 Snellen E presented at 7.5 M for15–20 s. To directly compare the PowerRefractor measures to the retinos-copy measures, the refractive power of the vertical meridian was calcu-lated from the overall sphero-cylindrical retinoscopy measures(J90 D Jsph sin2(�cyl ¡ 90°)). The PowerRefractor’s infrared light source illu-minates the fundus and the brightness of the reXex (pixel intensity slope)across the vertical meridian of the pupil is converted into refractive stateusing a built-in calibration function (Seidemann, SchaeVel, Guirao, Lopez-Gil, & Artal, 2002). We found that this function over-estimated the levelsof myopia and hyperopia when compared to our cycloplegic retinoscopy(see Fig. 1). Using the cycloplegic retinoscopy measures as a standard, anew calibration function was determined by converting PowerRefractormeasures back into pixel intensity slopes and then re-converted to refrac-tions using our calibration function (refraction D¡0.88 + 1.53 (pixel inten-sity slope)).

2.5. Filtering of the accommodative response

The accommodative response for each subject at each reading dis-tance was measured continuously for 10 min. The response was WlteredoZine to remove measurement artifacts due to blinks and Wxationbreaks outside of the text window. To remove the artifacts associatedwith blinks without erroneously removing any true accommodation, weWltered out refractive changes that were too fast to be considered physio-logical (>10 D/s) (Adrian Glasser, personal communication; CiuVreda &Kruger, 1988). These data were removed from the accommodativeresponse by an iterative algorithm that located diVerences greater than10 D/s between two data points and then removed the point that was fur-thest away from the mean accommodative response. Fig. 2 shows 60 s ofaccommodation for an individual before and after Wltering.

2.6. Analysis of the accommodative response

Several aspects of the accommodative response were identiWed andanalyzed. The mean error in the accommodative response relative to thetarget demand (i.e., lead or lag) was determined for each subject in 10 one-minute periods for each reading distance. Individual stimulus–responsefunctions were calculated using the three accommodative demands. Thevariability of accommodation response (determined from the standarddeviation of the response) was determined for these periods and an analy-sis of the power spectrum of the accommodative response was also per-formed.

2.6.1. Power spectrum analysisFourier analysis of the accommodative data from each minute of read-

ing was used to produce power spectra of each subject’s accommodativeresponse during reading. Prior to the fast Fourier transform the DC com-ponent was removed by generating a running average in 0.12 s increments(low pass Wlter). A Gaussian function was then applied to the Wrst and last7 s of data to remove high amplitude edge eVects. The 10 one-minute fastFourier transforms were then averaged to generate a single power spec-trum for each subject and the average power of low (LFC: 0.1–0.6 Hz),middle (MFC: 0.61–0.99 Hz), and high (HFC: 1.0–2.3 Hz) frequency com-ponents, which have been previously identiWed (Campbell, Robson, &Westheimer, 1959; Kotulak & Schor, 1986; Seidel et al., 2003; Winn, Pugh,Gilmartin, & Owens, 1990), was determined (see Fig. 3 for an example ofan individual power spectrum).

2.7. Statistical analysis

Repeated measures ANOVAs were used to determine if the variousaccommodative measures changed over time or with diVerent readingdemands. Additionally, correlations were used to determine whether rela-tionships existed between any of the accommodative measures and subjectrefractive state. Unpaired t tests were used to compare accommodativemeasures between the myopic and emmetropic groups. Statistical analysiswas performed using Statview (Abacus Concepts, Inc., Berkeley, CA), andsignal Wltering, power spectrum analysis, and graphical analysis was per-formed using KaleidaGraph (Synergy Software, Reading, PA).

Fig. 1. The PowerRefractor’s built-in calibration function over-estimatedthe amount of myopia and hyperopia compared to cycloplegic retinoscopy.

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3. Results

3.1. Accommodative responses

The average accommodative error (the diVerence betweenthe mean accommodative response and the target demand)observed at each of the reading distances was an accommo-dative lag. There was considerable inter-subject variability in

Fig. 3. Example of a power spectrum derived from fast Fourier transformsfor an individual (gray line) and a weighted mean curve Wt was applied(black line). The mean power of three frequency components; LFC (0.1–0.60 Hz), MFC (0.61–0.99 Hz), and HFC (1.0–2.3 Hz) were calculated foreach individual by the area under the curve for the corresponding frequencyranges and were normalized to the component frequency bandwidth.

the lag of accommodation at all reading distances (Fig. 4).The mean lag of accommodation for all subjects over the10 min reading period signiWcantly increased with closerreading distances (Fig. 4D, mean§SE, 0.69§0.08 D at 1.5 D;0.88§0.10D at 2.5 D; and 0.99§0.14 D at 3.5 D; repeatedmeasures ANOVA p <0.05). On average, the accommodativeerrors were greatest during the Wrst 2–3 min of reading andthen reduced (by approximately 0.2 D at the 2.5 and 3.5 Ddemands) and remained stable throughout the remainder ofthe reading period at all distances tested. One individualdemonstrated a substantial lead of accommodation at the 1.5and 2.5 D reading demand. This subject was later diagnosedwith an accommodative excess and was not included in thegroup analysis because of failure to meet the subject inclu-sion criteria of normal binocular vision.

In general, the lag of accommodation was not signiW-cantly correlated with the subjects’ refractive state(R2D0.05, pD0.39 at 2.5 D; R2D 0.02, pD0.59 at 3.5 D),although at the 1.5 D demand the lag of accommodationtended to be greater in myopes (R2D 0.17, pD 0.08) and themean lag of all myopes was greater than for emmetropes(mean§SE myopes vs. emmetropes, 0.84§ 0.08 D vs.0.56§ 0.09 D, unpaired t test p < 0.05).

There was substantial inter-subject variability in the slopesof the accommodative stimulus–response functions (deter-mined from the slopes of linear regressions) (range: 0.41–1.36,mean§SE, 0.85§0.06). There was no signiWcant diVerencebetween accommodative stimulus–response slope betweenmyopes and emmetropes (mean§SE myopes vs. emme-tropes, 0.92§0.09 vs. 0.77§0.07; unpaired t test pD0.28).

3.2. Variability in accommodation

The variability of the Wltered accommodative response foreach subject, measured as the mean standard deviation of theresponse, diVered substantially among the subjects and, on

Fig. 2. (A) Example of an accommodative response during 1 min of reading (horizontal line indicates the accommodative demand). The large myopicdeXections are artifacts from blinks. (B) The same accommodative response after data corresponding to blinks and gaze breaks outside the text windowwere removed.

E. Harb et al. / Vision Research 46 (2006) 2581–2592 2585

average, at each of the reading demands (Fig. 5). Examinationof each minute shows that, on average, the mean variabilitydid not change signiWcantly over the 10min reading period atany of the reading demands (ANOVA). The mean standarddeviation of the accommodative response increased signiW-cantly with closer reading demands (Fig. 5D, mean§SE,0.15§0.02D at 1.5D; 0.20D§0.02D at 2.5D; 0.30§0.04Dat 3.5D; ANOVA p<0.01). The variability of the accommo-dative response was proportional to the amplitude of theresponse (Fig. 6, R2D0.38, p<0.01).

Variability in an individuals’ accommodative responsewas related to accommodative demand and to refractivestate. Accommodative variability was proportional to thedegree of myopia at each of the three reading demands(Fig. 7, R2D0.49, p < 0.01 at 1.5D; R2D0.31, p < 0.05 at 2.5 D;and R2D0.34, p < 0.05 at 3.5 D). Furthermore, myopesshowed greater accommodative variability than emmetropesespecially at the closest reading demand (mean§SE myopesvs. emmetropes, 0.34§0.04 vs. 0.21§0.02; unpaired t testp < 0.05).

3.2.1. MicroXuctuationsThe mean power (D£ 10¡2) of the three frequency com-

ponents of accommodative microXuctuations increased sig-niWcantly with closer reading distances (Fig. 8, repeated

measures ANOVA; LFC, pD0.01; MFC, p < 0.05; HFC,pD0.05). The mean power of the microXuctuations for allfrequency components signiWcantly increased with increas-ing myopia at the 3.5 D demand (Fig. 9; LFC, R2D0.43,p < 0.05; MFC, R2D0.48, p < 0.05; HFC, R2D 0.50, p < 0.01),but not at the 1.5 and 2.5 D demands.

3.2.2. PowerRefractor control experimentsSeveral possible sources of variability in the PowerRe-

fractor measures were considered in a series of controlexperiments. Because we were concerned that the PowerRe-fractor readings might increase in variability at closer read-ing distances because of increased variability with steeperpixel intensity slopes, an analysis of uncorrected myopes(range: ¡0.25 to ¡5.0 D, nD 7) was performed. In thisexperiment, the subjects were instructed to look at a distanttarget (high contrast 20/100 Snellen letter presented at 6 m)while measures were made continuously for approximately15 s. A small but signiWcant increase in the variability (stan-dard deviation) of the measures with increasing myopiawas found (yD 0.07¡0.03x; R2D0.59; p < 0.05), but it wastoo small to account for the increase in variability ofaccommodation seen at closer reading demands. To deter-mine how much variability in the accommodative responsemight be due to measurement noise from eye movements

Fig. 4. The average accommodative response during the reading period diVered substantially between subjects at the three accommodative demands. Indi-vidual accommodative responses are shown as solid black lines. The dashed line indicates the response of a subject who demonstrated a lead of accommo-dation and was diagnosed with an accommodative excess. The straight horizontal line denotes the accommodative demand at each reading distance. Themean lag of accommodation (means § SE: 0.69 § 0.08 D at 1.5 D demand, 0.88§ 0.10 D at 2.5 D demand, and 0.99 § 0.14 D at 3.5 D demand, ANOVAp < 0.01) for the group at each reading distance.

2586 E. Harb et al. / Vision Research 46 (2006) 2581–2592

during reading we performed an analysis on a sample ofcyclopleged subjects (nD 23) to compare the diVerence inthe variability of measures made while Wxating on a neartarget (isolated letter) and while reading at two near dis-tances (28.6 and 66.6 cm). Since the subjects were unable to

Fig. 6. Linear regression demonstrates a proportional relationship(p < 0.01) between the mean accommodative responses and mean stan-dard deviation of the response averaged over the entire reading period forall subjects and all three accommodative demands.

accommodate, their right eye was fully corrected with anappropriate trial lens for each of the near targets while aninfrared Wlter was used over their left eye that allowed thePowerRefractor to measure Xuctuations in refractionsassociated with changing eye position. The diVerence in thestandard deviation of the response between Wxating andreading conditions was not signiWcant at the 1.5 D demand(mean§SE looking vs. reading, 0.17§0.03 vs. 0.23§ 0.03,paired t test pD0.53). At the 3.5 D demand, the variabilityin the response was signiWcantly less during reading com-pared to Wxating (mean§SE looking vs. reading 0.32§0.04vs. 0.18§ 0.04, paired t test p < 0.01), suggesting that eyemovements during reading are not a source of increasedvariability.

3.3. Fixation breaks

The number of Wxation breaks over the reading period wasanalyzed for each subject. While there were large diVerencesbetween individuals, on average there was a signiWcantincrease in the number of Wxation breaks at the 3.5D demand(Fig. 10, mean§SE, 13.07§5.46 at 1.5D; 12.86§6.13 at2.5D; 32.00§11.20 at 3.5D; repeated measures ANOVA,p<0.05). Myopes had signiWcantly fewer Wxation breaks thanemmetropes at the 2.5 and 3.5D reading demands (Fig. 10,mean§SE, myopes, 1.00§0.63; emmetropes, 28.50§11.92 at

Fig. 5. Variability of the accommodative response (measured as mean standard deviation (SD)) per minute of reading diVered substantially at each of theaccommodative demands. Individual data (dashed lines (myopes) and solid lines (emmetropes)). The mean variability for the entire group signiWcantlyincreased at the closer reading distances ((mean § SE) 0.15§ 0.02 at 1.5 D demand, 0.20 § 0.02 at 2.5 D demand, 0.30 § 0.04 at 3.5 D demand).

E. Harb et al. / Vision Research 46 (2006) 2581–2592 2587

2.5D, ANOVA p<0.05; myopes, 1.83§1.25; emmetropes,46.33§19.05 at 3.5D, ANOVA p<0.05).

4. Discussion

Accommodative behavior associated with the type ofnear work commonly seen in school-aged children has beensuspected to be a factor in the development of myopia. Sev-eral investigators (Abbott et al., 1998; Gwiazda et al.,1995a, 1993; Jiang, 1997) have speciWcally hypothesized

that large lags in accommodation degrade retinal imagequality by producing hyperopic retinal defocus, and mayaVect eye growth and refraction in much the same way thatnegative lens-rearing aVects eye growth and refraction inanimal models (Graham & Judge, 1999; Hung et al., 1995;SchaeVel et al., 1988; Whatham & Judge, 2001). Reading isa sustained near work task that uses unique visual stimuluscharacteristics and requires extraordinarily long periods ofvisual attention, serial saccades, and accommodation to anear target. Accommodative errors, and the associated

Fig. 7. Linear regression analysis demonstrating the relationship between subject refractive error and mean standard deviation of the accommodativeresponse at each of the reading demands (correlations p < 0.01 at 1.5 D, p < 0.05 at 2.5 D and 3.5 D).

Fig. 8. Mean (§SE) power of each of the frequency components calculated from the Fourier derived power spectra for each subject at each demand(repeated measures ANOVA, LFC pD 0.01; MFC p < 0.05; HFC p D 0.05). The mean power of each frequency component has been normalized to the fre-quency bandwidth.

Fig. 9. Linear regression showing a proportional relationship between subjects refractive error and the mean power of accommodative microXuctuations,for all three frequency components, at the 3.5 D reading demand (correlation LFC and MFC p < 0.05, HFC p < 0.01). The power of each frequency com-ponent was normalized to the component frequency bandwidth.

2588 E. Harb et al. / Vision Research 46 (2006) 2581–2592

retinal defocus during sustained periods of reading mightmake a child’s eye more vulnerable to the eVects of hyper-opic defocus. In this paper, we examine several aspects ofaccommodative behavior that may be additional risk fac-tors for myopia development.

4.1. Accommodative lags

Accommodative lags in young progressing myopes arelarger than in emmetropes (Gwiazda et al., 1993; Gwiazdaet al., 2005; He, Gwiazda, Thorn, Held, & Vera-Diaz, 2005;Nakatsuka et al., 2005), but adaptations within the accom-modative system appear to increase the accommodativeresponse so that in adults with stable myopia the mean lagis not diVerent from that of adult emmetropes (Abbottet al., 1998; Nakatsuka, Hasebe, Nonaka, & Ohtsuki, 2003;Seidemann & SchaeVel, 2003). Our Wndings are consistentwith this because there was no statistical diVerence in theaccommodative lags between myopes and emmetropes.Although we Wnd large diVerences in accommodative lagsbetween subjects, the mean lag during extended periods ofreading was similar to that shown in other studies duringbrief periods of accommodation (Gwiazda et al., 1993;McBrien & Millodot, 1986; Nakatsuka et al., 2003, 2005).We also observed that, after an initial period of 2–3 min, thelags were reduced slightly and then remained relatively con-stant over the remaining reading period. A reduction in thelag of accommodation within the Wrst few minutes of read-ing has been previously observed and has been hypothe-sized to result from increased output of a slow, blur-driven,accommodative response mediated by the sympathetic ner-vous system (RosenWeld & Gilmartin, 1998a; Schor, Kotu-lak, & Tsuetaki, 1986). Such adaptation may increase theaccuracy of the accommodative response during a sus-tained reading period and ultimately increase subjectiveclarity. Vera-Diaz, Gwiazda, Thorn, and Held (2004) alsoreported an increase in accommodative gain in myopes fol-lowing viewing of a blurred stimulus that could not becleared by accommodation. This adaptation was hypothe-

sized to be a result of diVerences in the use of sensory blurcues between myopes and emmetropes.

We also found that, on average, the lag of accommoda-tion increased signiWcantly with closer reading distances, con-sistent with earlier reports (Charman, 1999; Gwiazda et al.,1993; Seidemann & SchaeVel, 2003). Interestingly, some ofthe subjects in our study showed particularly large lags ofaccommodation (>1.0 D), but this did not seem to compro-mise their ability to read, raising questions about how thesubjects were able to read through substantial hyperopicdefocus. We speculate that large accommodative lags may betolerated during reading in certain individuals for severalpossible reasons. (1) High contrast and low spatial frequencycontent (near the peak of the contrast sensitivity function)are typically found in text and does not appear to requireparticularly accurate accommodation to be visible (Tucker &Charman, 1987; Ward, 1987). Studies have also shown thatreading speed and word recognition are not aVected evenwhen text contrast is reduced 30% (Legge, Kersten, & Bur-gess, 1987; van Nes & Jacobs, 1981). (2) Optical aberrationsin the eye may also play an important role in a subject’s abil-ity to read through signiWcant defocus (for a recent review seeCharman, 2005). Increased aberrations induce a greaterdepth of focus that would impart greater perceived clarity toa defocused retinal image. (3) Adaptations to blur (Mon-Wil-liams, Tresilian, Strang, Kochhar, & Wann, 1998; RosenWeld& Gilmartin, 2004; Webster, Georgeson, & Webster, 2002)may be greater in some individuals, resulting in a variety ofaccommodative lags, and could account for the ability toread through a signiWcant lag of accommodation with per-ceived clarity.

4.2. Accommodative Xuctuations

Although the accommodative lags of the myopic sub-jects were similar to those of the emmetropic subjects in ourstudy, the variability of their accommodative responses wassigniWcantly greater as shown by several criteria. Our datashow that accommodation during extended periods of

Fig. 10. (A) The number of Wxation breaks away from the text windows was signiWcantly greater at the closer reading demand (repeated measuresANOVA: p < 0.05). (B) Myopes had signiWcantly fewer Wxation breaks at the 2.5 D and 3.5 D demands compared to emmetropes (ANOVA: p < 0.05).

E. Harb et al. / Vision Research 46 (2006) 2581–2592 2589

reading is proportionally more variable in myopes in termsof both the standard deviation of the accommodativeresponse and the power spectra of accommodative micro-Xuctuations. Both measures vary greatly between individ-ual subjects but, overall, show increases with increasingaccommodative demand. Increases in accommodativemicroXuctuations have also been observed with increasingaccommodative demands during brief periods of accommo-dation by others (Campbell et al., 1959; CiuVreda & Kru-ger, 1988; Day et al., 2006; Kotulak & Schor, 1986; Plainiset al., 2005; Seidel et al., 2003) and could be a product ofsignal-dependent noise (Harris & Wolpert, 1998). DiVer-ences in the variability of the accommodative response withthe subjects’ refractive state, however, suggest a morecomplex relationship. We hypothesize that increased depthof focus in myopes, possibly because of increased aberra-tions (Charman, 2005), may be responsible for a reductionin blur sensitivity (RosenWeld & Abraham-Cohen, 1999)and lead to increased accommodative variability (Dayet al., 2006; Seidel et al., 2003). Myopes have been shown innumerous studies to have increased astigmatism and higherorder aberrations compared to emmetropes (Cheng et al.,2000; Collins, Buehren, & Iskander, 2006; He et al., 2002,2005; Kirwan, O’Keefe, & Soeldner, 2006; Marcos,Moreno-Barriuso, Llorente, Navarro, & Barbero, 2000;Simonet, Hamam, Brunette, & Campbell, 1999; Sun, Sun, &He, 2000, but see Llorente, Barbero, Cano, Dorronsoro, &Marcos, 2004), which may be the result of poor compensa-tion of corneal aberrations by internal optics (Benito &Artal, 2004). In addition, changes in the eye’s aberrationshave also been reported to occur during accommodation.These changes could aVect the accuracy of the accommoda-tive response during reading. In particular, positive spheri-cal aberrations have been reported to become morenegative during accommodation and would increase thedemand needed to produce a clear retinal image (He,Burns, & Marcos, 2000; Plainis et al., 2005). Although thisvaries widely among studies (Charman, 2005; Cheng et al.,2004; He et al., 2000; Ninomiya et al., 2002; Vilupuru,Roorda, & Glasser, 2004), it has been reported to occur to agreater degree in myopes during accommodation and aftersustained periods of reading (Buehren, Collins, & Carney,2005; Collins et al., 2006; He et al., 2000). Finally, themicroXuctuations of higher order aberrations have beenshown to have similar frequency characteristics to accom-modative microXuctuations (Zhu, Collins, & Iskander,2004) and both may be related to the dynamics of accom-modation during sustained reading.

Our data suggest that the increased variability of theaccommodative response observed in myopes is speciWc tothe operation of the accommodation controller, and possi-bly the accommodative plant, and not to the generalincrease in variability associated with increasing demands.In this study, both myopes and emmetropes show approxi-mately the same average accommodative response for agiven target. Therefore, accommodation in myopes appearsto possess characteristics that result in greater Xuctuations

without changing the average accommodative response.Adult myopes are less sensitive than emmetropes to thedefocus cues that drive accommodation (RosenWeld &Abraham-Cohen, 1999; Thorn, Cameron, Arnel, & Thorn,1998), although myopic children may have similar blurdetection thresholds to age-matched emmetropes (Schmid,Iskander, Li, Edwards, & Lew, 2002). The accommodativeresponse of young myopes is reduced (lags are greater)when their myopia is progressing but improves to the levelof emmetropes as myopic progression slows and stabilizes(Abbott et al., 1998; Gwiazda et al., 1995a; Nakatsukaet al., 2003) suggesting accommodative gain adjustments.Pairing adaptable system gain with decreased sensitivitywill result in response instability in the accommodativecontroller, as in any servosystem. Finally, it is also plausiblethat the shape of the myopic eye aVects the operation of theciliary muscle and may aVect the accommodative response(Mutti et al., 2000) by increasing the tension on the ciliaryzonules and the accommodative eVort for a given demand.In theory, the increased accommodative strain put upon theaccommodative plant could also cause an increase in thevariability of the response.

The increases in accommodative variability and lags,associated with closer reading demands may have impor-tant clinical implications. Individuals preferring closerreading distances may be more susceptible to myopiabecause both the Xuctuations and lags are greater. Theassociated increases in hyperopic blur may signal increasedeye growth (Bartmann & SchaeVel, 1994; Flitcroft, 1998;Goss & Wickham, 1995; Hung & CiuVreda, 2000; Jiang &Morse, 1999). Myopic children have habitually closer work-ing distances than emmetropic children (Haro, Poulain, &Drobe, 2000) and myopia progression is signiWcantlygreater in children with closer near working distances(Parssinen & Lyyra, 1993). Moreover, the Correction ofMyopia Evaluation Trial (COMET) has recently reportedthat children wearing progressive addition lenses who had alag of accommodation greater than 0.43 D and a closerthan normal reading distance (<31.2 cm) had a signiWcantlygreater treatment eVect in the reduction of myopia com-pared to single vision lens wearers (a 0.44 D diVerence overthree years) (Gwiazda, Hyman, & Norton, 2004). Interest-ingly, we also observed that myopes had signiWcantly fewerWxation breaks than emmetropes at the closest reading dis-tance, suggesting that breaks from reading at a close dis-tance may have a protective eVect. This is consistent withthe fact that even very brief periods of myopic defocus havebeen shown to inhibit compensatory axial growth to sus-tained periods of hyperopic defocus in animal models (Zhu,Winawer, & Wallman, 2003).

5. Conclusion

In this study, we show that in adult subjects with stablemyopia, the average accommodative response amplitudeduring an extended period of reading is virtually identicalto that of adult emmetropes. We Wnd, however, that there is

2590 E. Harb et al. / Vision Research 46 (2006) 2581–2592

more variability in myopes, which is consistent with thehypothesis that myopes are less sensitive to defocus. Whilethe small Xuctuations in the accommodative response maybe individually too small to stimulate eye growth, temporalintegration of the Xuctuations over periods of sustainedreading may be suYcient to produce a blur signal that maylead to myopia. Investigation in individuals with progress-ing myopia, particularly children, is necessary to determinewhether these diVerences are risk factors for the develop-ment of myopia.

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