A PHOTOREFRACTIVE STUDY ACCOMMODATION

OF INFANT

OLIVER BRADDICK,JAXETTEATKINSON and JEYINIFER FRENCH Psychological Laboratory, University of Cambridge, Cambridge. England

HOWARD C. HOWLAND Sections of Neurobiology and Behavior and Physiology. Cornell University. Ithaca, New York 148JO. U.S.A. (Receiced

3 April

1979)

Abstract-The technique of “photorefraction” has been used to investigate the refractive state of freely accommodating infants. when presented with targets at distances up to 150 cm. Groups of infants were aged from birth to 1 yr. Ail infants tested at six months and older. and most 2-3 mth infants. showed the ability to accommodate correctly on targets at I SOcm and closer. Newborn and 1mth infants could accommodate more accurately at 75 cm and closer than they could at 150 em. Many infants who did not consistently accommodate for 150 or 75 cm distant targets nonetheless showed fluctuations of accommodation that included the appropriate distance. 62% of our infant sample showed a significant degree of astigmatism. The errors of accommodation observed are insufficient to be the limiting factor on reported values of infant acuity. We conclude that accommodative errors may instead be the consequence of infants’ limited ability to process the retinal image so as to detect incorrect accommodation. and possibly also of limitations of visual attention for targets further than I m.

IWRODUCW3N

A number of recent studies have investigated the development of visual acuity and contrast sensitivity in infancy, using behavioural and evoked-potential techniques (Fantz et af., 1962; Marg er a[., 1976; Hatter et al., 1977; Atkinson et al., 1977; Banks and Salapatek, 1978; Sokol, 1978; Dobson and Teller. 1978; Pirchio et ai., 1978). These studies show a rapid improvement in spatial vision over the first few months of life. However, how far this improvement is due to changes in the quality of the optical image formed on the infant’s retina, and how far to development of the neural structures of the retina and visual pathway, has not been determined. In this paper we investigate how well the freely accommodating infant eye forms a sharp image of a fixated target at various distances. The interest of this question Iies in (i) enabling us to separate neurai and optical Pactors in the development of visual performance, and hence to relate performance data to questions on the normal and abnormal development of the structures of the visual system; (ii) beginning the developmental exploration of a particular sensory-motor system: the control of the eye’s accommodation by the information in the retinal image and (iii) possible understanding of the origins in early life of ametropias and emmetropia. Previous approaches to the problem have been: (i) estimates of the relaxed refractive state of the infant eye, obtained under cycloplegia. An extensive

body of data shows average hypermetropia 1-2 D in early infancy, decreasing to near emmetropia by adolescence (Borish, 1970; Duke-Elder, 1949). (Some part of this hypermetropia may be due to the artefact of retinal thickness pointed out by Glickstein and Millodot, 1970.) Such refractions. however, do not tell us how. well focused the infants’ eyes are in normal vision, without knowledge of the range of accommodation and of how accurately infants in fact accommodate within this range; (ii) the only published direct study of natural accommodation in infants has been carried out by Haynes et al. (1965) using dynamic retinoscopy. They report that the function relating accommodative response to target distance was nearly fiat at age 1 mth. and increased in slope until it approximated adult performance (accurate accommodation over the range O-5 D) at 4mths. These data have been generally interpreted as the I mth old infant having “fixed focus” at around 2Ocm. Recently Banks (1978) has performed a similar study with generally similar results, though he shows, age for age, somewhat better accommodative performance than Haynes et al.; (iii) two studies of i-2mth old infant acuity (Salapatek et al., i976; Atkinson et a!., 1977) have found no change in measured acuity over a range of distances. These results make it unlikely that measured values of infant acuity have been limited by infants accommodating at the wrong distance for the stimulus, The present study was undertaken to extend these results with measurements of free accommodation using a new technique; “photorefraction” (Howland

1319

1320

OLI\ER BRADDICK. J,A>ETTE .\TW.SOS. JESSIFER FRESCH md

and Hou-land, 197-I). With this technique, a flash photograph of the subject’s eyes is taken using a special camera attachment. Measurements on this photograph give an estimate of the optical defocus of the e>es relative to the camera distance. Comparison of‘ photorefraction tire methods

with alternutiie

refrac-

The significant characteristics of photorefraction are that it gives information about the instantaneous refractive sfate of a freely accommodating subject. in two orthogonal meridians and for both eyes simultaneously. It indicates the degree of defocus relative to the camera but does not give directly the sign of that defocus (relative hypermetropia or myopia). Alternative methods for the objective assessment of refractive state are: (i) infin-red oprometers (Cornsweet and Crane, 1970; Charman and Heron. 1975). These give data of considerable precision and are the only method that permits continuous monitoring of fluctuations in accommodation. However. they require a degree of maintained accurate fixation which is quite impractical for infant subjects: (ii) retinoscopic methods: (a) retinoscopy under cgcloplegia is routinely used for clinical refraction of infants of all ages. However, the cycloplegia renders the study of active accommodation impossible; (b) near retinoscopy (Mohindra. 1977a.b) involves no cycloplegia but is conducted in darkness; the retinoscope lamp is believed not to be an adequate stimulus for accommodation, so a resting state of accommodation is taken up (Leibowitz and Owens, 1975) bearing an approximately fixed relation to the cycloplegic refraction. It is in use for an extensive study of infant refraction (Mohindra et al., 1978a,b) but again does not yield information on active accommodation; (c) dynamic retinoscopy, i.e. retinoscopy of the freely accommodating eye with a prominent target for accommodation. This was used in studies of infants by Haynes er al. (1965) and Banks (1978). The advantage of these procedures over photorefraction is that the direction of the reflex movement, and/or the sign of the lenses inserted to nullify it, directly indicate whether the eye is focused in front of or behind the retinoscopist’s working distance. The disadvantages are: (a) even a single retinoscopic measurement takes a few seconds. Retinoscopy cannot say anything about variations more rapid than this and (except under cycloplegia) they may introduce uncertainty into the measurement. Such variations may be significant in infant vision and may be sampled by photorefraction. The need to sustain the infant’s fixed attention for an adequate time is the principal problem with infant retinoscopy; photorefraction allows the measures to be made even at brief moments when the infant is judged to be attending; (b) comparisons of refraction in different axes (astigmatism) and in the two eyes (anisometropia) require successive retinoscopic measurements and SO may be contaminated by fluctuations in accommo-

HOWARD

C.

HOWLA~D

dation. In photorzfraction all these measurements for the same moment in time ma! be derived from J single photograph: (c) photorefraction yields its raw data in a permanent form. which can be compared between different photographs and inspected b! an\ observer. Retinoscopy is dependent on the re;inoscopist’s judgement of a fugitive image. It should be emphasized that photorefraction. like dynamic retinoscopy. yields information about the accuracy of active accommodation at a given target distance. This is a rather different question from the esrimation of the refraction of a relaxed eye. which is ths aim of cycloplegic and near-retinoscopq. However. the position of the far-point will be one of rhe constraints on the accuracy of accommodation. and ma;. often be estimated from a photorefractive series. An additional feature of photorefraction is that ir measures the point-spread function of the optics oi the eye. and will reveal image blur whether due to dioptric defocus or to Retinoscopy, in contrast.

any other optical measures dioptric

causs.

defocus specifically. Photorefraction in principle therefore bears a closer relation than retinoscopy to questions of optical effects on acuity: retinoscopy to questions of refractive error, insofar as these may be dissociated. 4IETHODS

The photorefractive attachment consists of the tip of 1 fiber-optic light guide in the center of a ring of four pieshaped segments of cylinder lens with tangentiallq oriented axes. The attachment screws onto the front of the wide aperture (Jl.2, 55 mm) lens of a 35 mm single-lens reflex camera. The fiber-optic tip acts as a light source which 1s imaged on the subject’s retina. Light returning from this image is photographed through the attachment whit> creates a four-armed star image at the film plane. If the fiber-optic tip is in focus on the retina. it is also conjugate with the retinal image for light returning from the retina_ and little or no light escapes round the tip to reach the film plane; consequently the star image has short arms or is absent. If. however. the retinal image and the photorefractive attachment are not conjugate. the returning light extends over the cylinder lens segments and a star image is formed whose arms vary in length with the dioptric defocus of the eye relative to the camera (Fig. 1). In th: case of an astigmatic eye. the lengths of the orthogona! pairs of arms in the star image differ according to the difference in refractive power in the corresponding meridia. Figure 2 illustrates examples of the images obtained. The construction, use and theory of the photorefractor are discussed in detail by Howland and Howland (1974) and a more complete theory for near working distances is described by Howland et al. (in preparation). The technique used in this study differed from that described by Howland and Howland in three ways. First. the light source feeding the fiber-optic guide was an electronic xenon flash rather than a tungsten illuminator and shutte:. This was more convenient and also avoided the use of a long (0.25 set) exposure in which our infant subjects might have moved. Its intensity at the 1.5 m camera distance was approximately that used in the original method (Howland and Howland. 1974), but at 0.75 m we inserted an 0.7 neutral density filter between the flash gun and proximal fiberoptic tip. Secondly, the photographs were taken on a color transparency film (Kodak High Speed Ektachrome. uprated in

1321

A photorefractive study of infant accommodation

Cylmdratl

Blurred

wnctge

Of so”rce

on

lens

segments

fundus

Fig. I. Optics of the photorefractor. Light from a fibre-optic light guide centered in array of 4 cylinder lenses (axes tangential) is focused on the retina of the subject who is focused myopically with respect to the camera. Light returning from the retina to the camera falls on the cylinder lens segments and is focused into a cross-shaped pattern. with the lengths of the cross arms being directly proportional to the degree of defocus in the corresponding meridian. The dioptric defocus calculated from reflexes of a given length depends markedly upon the diameter of the subject’s pupils. Pupil size was measured using a fiber-optic flash source centered in the camera lens. without the sur(a) the retinal reflexes were more readily distinguished rounding cylinder lens segments of the photorefractor. This from the background of the subject’s face. etc. (It was not yields a normal photograph of the subject in which the feasible to photograph infant’s eyes through a black mask pupils are flooded with reflected light. so their diameter as described by Howland and Howfand, 1974); may easily be measured under the same conditions of illu(b) the white light in the reflexes originating in the retinal mination as used in the photorefractive pictures. images of the flash source could be distinguished from the In studying the focusing ability of the infants we found it more broadly distributed scattered light. which was reddish useful to work at 1.5 and 0.75 m. These distances are closer in color. This red diffusely scattered light is probably rethan the 2m of the original paper and some approxisponsible for the long plateau of the linespread function mations given for interpreting the length of the reflexes are which a number of investigators have noticed (Campbell no longer valid at these closer distances. Accordingly, we and Gubisch, 1966: Rohler er al.. 1969); calculated by numerical ray tracing the extent of the pho(c) color differences in the reflexes sometimes gave a clue torefractive traces we would obtain for various pupil sizes. as to the direction of refractive error. degrees of defocus and camera-to-subject distances. Results of these calculations are given in Fig. 3a and 3b. The comThirdly. photographs were taken at two different putational technique will be discussed in detail in Howland camera-to-subject distances (I.5 and 0.75 m). er al. (in preparation). The length of the star arms gives the magnitude of any In measuring the star arms from the photorefractive defocus relative to the camera distance. but not its sign. positives we mounted and projected these as 35 mm slides Howland and Howland (1974) show how comparison of at 25X magnification. We then measured the diameters of two photographs taken through different color filters allow the star arms directly from the projection screen with a the sign to be inferred from the chromatic abberation. millimeter ruler or calipers. This was done with the person However, this method was not appropriate for the present at the screen indicating the distance measured while being study. because there was no assurance that the infant submonitored by observers at a distance of 3-4m from the jects would maintain constant accommodation for two SUCscreen. This was necessary because it was often easier to cessive photographs. While the main results to be presee the bounds of the reflex when it subtended a narrow sented below do not depend on any inferences about the visual angle than a large one. sign of any defocus observed. nonetheless a number of These measured diameters were then converted to radii sources of information were available about the direction of the star arms at the film plane and via the calibration of refractive errors: graphs of Figs 3a and b into diopters defocus. Because the slopes of the calibration curves for any one (i) dynamic retinoscopy was performed with some subpupil size and camera distance differ slightly’ depending jects, usually at a distance of 50 cm; (ii) color effects attributable to chromatic abberation upon whether the eye is myopically or hyperopically focused relative to the camera, we always evaluated astigwere visible in the reflexes on some photographs. These matisms as if both meridia fell on the low slope (relative were most useful in cases of astigmatism when there was myopic) side with a view towards under- rather than oversometimes a difference in color between the star arms in estimating the cylinder errors. .orthogonal directions. processing to 400 ASA) rather than black-and-white film. It was found that the use of colour lilm made the visual interpretation of the images considerably easier because:

OLIVERBRADDICK. JALETTE ATKNOX. JEVSIFER FRESCHand Hou.\rrv C

I32

HO~L.A~D

tion of 31 adults most oi whom were myopic and or asttg matic. Each subject was both subjectively refracted and and the photorefractive photorefracted. traces were measured in the u~udi manner. Of these 62 eyes. 19 showed a cylindrical error of 0.‘5 D or more b! subjective refraction: IO showed a c>hndrtcal error oi at least thts size bv photorefraction. Fewer large astigmatisms were detected b: photorefraction than b> SubJecttve refraction because of vtgnztting b> the edges of the camera )ens in cases where asttgmattsm was compounded with a large spherical error. and because of SubJeCts compromising the astigmatism (focusing one meridian in front of and the other behind the camera). This impltes that our results are I~hel! to underestimate rather than overestimate the incidence of infant astigmatism. The correspondsncr between net spherical defocus as measured by photorsfracrton and that estimated from subjective refraction by the equation: Net spherical deiocus = sphere - (cylinder 2) - (1 working distance in meters) is gtven in Fig. 4. it will be seen that in the interval between 0 and 3 D low values of net spherical defocus as predicted bt subjective refraction are somewhat overestimated by photor~fra~tion at I.5 m. This may be due to the tendency of the subjects to shift their accommodation to a slightly more myopic resting accommodatton under the subdued lighting condittons of the test. In any event this would lead to a slight underestimation of the number of infants able to focus at I.5 m. The photorefractive method does not discriminate between degrees of defocus greater than 3 D. due to vignetting by the edges of the camera lens,

In order to compute a mmimum estimate of the amount of astigmattsm indicated b!. a particular photograph we normally subtracted the dioptrtc magnitudes of orthogonai traces. as computed from the cahbration graphs. In rare exceptions. where we had unambiguous evrdence from the color of the traces that one meridian was focused in front of and one behind the camera. the dioptric magnitudes were added, Again. this procedure provided a mmimum estimate of the astigmatism about the two orthogonal meridians, because it may well be that cases of mtned asttgmatism relative to the camera were missed. Sometimes both sets of orthogonal traces. i.e. 0. 90 and 45. 135’ showed an astigmatism, indicating that the axis was somewhere between these meridia. In this case we solved for the true axis and magnitude of the astigmatism; otherwise, we simply took as the astigmatism the maximum of the differences between orthogonal meridia. In order to validate our new procedures for photorefractive measurement we adv,ertised for and refracted a popula-

Procedure

!I

1

-5

-6

-3

-2

-1

Relative

0 defocus

2

1

j

,

,

3

L

f

Infants were tested seated on the knee of either the mother or an experimenter, facing the camera. The experimental room was illuminated by a 60 W desk lamp directed away from the subject and target. giving a general level of illumination in the low photopic range. Since it is well known that the refraction of adult eyes varies in an unsystematic manner off the visual axis (Ferree and Rand. 1932). we took considerable care to use only photographs taken on or very near the visual axis. For

[Q]

7

Relative

Fig. 3. Star arm camera distance. camera. The sign in the construction tracing analysis.

defocus

6

5

[D]

radius at film plane vs diopters defocus for (A) 1.5 m camera distance and (B) 0.75 m Positive values of defocus indicate focus in front of the camera, negative behind &he of the asymmetry in the curve is due to the fact that positive cyIinder tenses were used of the photorefractive attachment. The curves were calculated from a numerical ray The different curves correspond to different pupil sizes (parameter indicates pupil diameter in mm.)

m

w

a

0

1323

A photorefractive

1325

study of infant accommodation

camera as target. The order in which the different conditions were used was varied from infant to infant. although to avoid prolonging the intervals between pictures all photographs involving one camera distance were taken before the other for a particular infant. All infants were tested in a calm and alert state. If an infant became too tired or fussy to complete the series in one session (most common with 1 mth or younger infants). the series was completed in a second session within a few days. Subject sample

All infants except the neonatal group were volunteers from the Cambridge City area recruited by distribution of leaflets in the maternity hospital. well-baby clinics and general practitioners’ offices. The leaflet stressed the need to study normal visual development and did not ask for visual family histories. The neonates (aged O-9 days) were recruited and tested in the Cambridge Maternity Hospital, the essential qualifications for testing being an alert and calm healthy neonate. They came from a wide catchment area with diverse socio-economic backgrounds. All parents were told the purpose of the tests. All infants had normal birth histories and were not more than IO days premature. Two infants were studied longitudinally over the course of the first year of life and are discussed separately in the results section. The age distribution of the infants used in the study is given in Table I.

I

I

2

Photorefraction

3

L

ID I

RESULTS

Fig. 4. Comparison of net spherical defocus as measured by photorefraction and estimated from subjective refraction of 31 adult subjects (each eye plotted separately). The vertical lines indicate the useful limits of photorefractive measurements for various pupil sizes at 1.5 m distance and a 46 mm camera aperture. photographs taken with the infant fixating at the camera distance. the camera operator was the visual target; with face close to the camera, he or she attracted the infant’s attention by calling, shaking brightly colored rattles, peekaboos and other attention-seeking activity. and operated the camera when he or she judged the infant to have established eye-to-eye contact. For other fixation distances. the infant was judged to have acquired the fixation target (a rattle) when it was actively followed with eye movements: the photograph was taken when the infant had tracked the target to a position where eyes, target. and camera were approximately in line. Spoiled pictures which did not meet these criteria were noted in the protocol and rejected, We estimate that our refractions were within 2.5’ of the visual axis at the 1.5 m camera distance, and within 5’ at the 0.75 m camera distance. A series totalling 15-25 photographs was taken for each infant, including one or more pupil photographs, pictures at each of the two camera distances, and pictures with the photorefractor oriented either horizonta!-vertical or obliquely. Usually 8 or 9 photographs were taken at each camera distance, at least half of theie being with the

For each infant an assessment was made of the degree of defocus when fixating at camera distances of 75 and 150 cm. Figs 5 and 6 plot the percentage of infants in each age group who met a criterion of being “in focus” at these two distances. For the 75 cm distance this criterion is determined by the “dead zone” within which the reflexes are vignetted by the fiber-optic head (see Figs 3a and b). Any photograph where the star arms in one or both meridians were less than 0.3 mm radius was taken as “in focus”. This actually defines an interval of focus extending over 1.2 D, almost entirely in front of the camera. At 150 cm the dead zone is smaller, and a criterion of 0.4 mm star arm radius. corresponding to 0.6 D in front of the 0.3 D behind the camera, could be adopted. This, the most stringent criterion used, is referred to as criterion A. To ensure comparability bet.ween our data at the two distances, we also assessed the 150cm photographs on two other criteria. Criterion 13 had a total range of 1.2 D, the same as that for 75 cm criterion. However, because this includes star arm lengths that are well out of the dead zone, part of the range is in front of and part behind the camera. Criterion C had. like the 75 cm criterion, a 1.2 D range in front of the camera; however, it also

Table 1

Age Neonates I mth 2-3 mth 68 mth 9-12mth Total

Infants showing astigmatisms of

Astigmatic

Meridional difference in

Total

Astigmatic

infants

infants

0.75 D

l-2D

>2D

eyes

O-90”

45-135’

Both

15 16 36 I4 12 93

7 11 24 10 6 58

3

4 7 15 7 2 35

0 3 6 0 2 II

12 22 46 18 12 110

8 14 34 14 7 77

2 4 2 0 2 10

2 4 10 4 3 23

: 3 2 I2

1326

OLIVER BWDDICK.

I

month

JASETTE ATWSOS.

32

12

2-3 months

6-6 months

JEMIFER

9

Age of infant 5

Fig. 5. Percentage of infants in each age group showing “consistent” and “inconsistent” focusing at a camera distance of 75 cm. The number of subjects in each group contributing to the data is indicated at the top of the figure. 0 q

FREXH

and Ho% ~RD C

HOWLAND

Included a considerable dtoptric range behind the camera. Criteria B and C cannot be stated in millimeters star arm radius because. unlike criterion .-t. the. jhovved a marked dependence on pupil size. In Figs 5 and 6 some infants have been categorized as ‘-inconsistent”. Bk this vve mean that on at least one photograph (out of 34 taken with the target at the camera) the images met the “in focus” criterion, but this was not so for others taken at the same camera distance. Such a result shoas a muscular capability to focus at the distance involved. but not consistent performance in doing so. A few infants for whom only a single interpretabls photorefractive picture was obtained with fixation on the camera at a given distance could not be classified as “consistent” or “inconsistent” if that picture met the criterion of focus: such infants were therefore omitted entirely from the analvsis for that distance. As can be seen from Fig. J. most infants of one month or older shoued consistent focusing at 75 cm. For each infant ue also examined photographs taken at a camera distance of 75 cm with target distances between 75 and ‘Ocm. .AII but a very few oi the infants who were “in focus” at 75 cm also shovvsd progressive defocus relative to the camera for targets closer than 75 cm. indicating an accommodative response at this range. At 150 cm (Fig. 6) the percentage of consistentl> focusing infants is much lower in the three younger age groups. This is not simply a consequence of the use of the more stringent criterion .-I. Figure 6 also shows the data for these three age groups based on the criteria B and C which are designed to be more

Inconsistent consistent

I6

A

B

1-9 days

C

ABC

I month

A

B

C

2-3 months

ABC

6-8 months

A

B

C

9-12 months

Age of infants

Fig. 6. Percentage of infants in each age group showing “consistent” and “inconsistent” focusing at a camera distance of 150 cm according to the criteria described in the text. The number of subjects in each group contributing to the data is indicated at the top of figure.

A photorefractive study of infant accommodation

comparable with the 75 cm data. Even on criterion C, which is in fact weaker than the 75 cm criterion. considerably fewer of the young infants showed either

2.5

consistent 15 cm.

1.5-O

or inconsistent

focusing

LO-

all infants over 2-3 mth. and many in the 2-3 mth group. were able to focus consistently at 150 cm. Even among the youngest age groups inconsistent focusing at I50 cm was often

In Table 1 we present the results of our minimum estimates of astigmatism from the photorefractive pic-

tures of 93 infants. (Most of these data was published in graphical form in a preliminary report of part of this study (Howland er al., 1978).) In the last three columns we show the distribution of astigmatism in terms of the principal meridians of difference in defocus. Most of the eyes showed cylinder axes of close to 0 or 90” (70%). another 9% showed oblique astigmatism with cylinder axes close to 45 or 135’. and 21% showed astigmatism which lay between these meridia.

l

0

3

. 0

0

.5. I 0

,,. 2

1

3

occom.ot 75. . . . accom at150 0 .a.

, ., 5 6 7 Agelmonthsl . . . . ‘

6

, 9

, 10

1

(112

. .

3.0.•

6

2.5.o

.c 4

2.0.

Infant B 8

0

1.5. E 5

.

1.0.

. 0

0

0

.5-

0 .

L

0

1

. .

2

3

L

5

6

7

6

9

10

11 12

Age tmonthsl

. .

. .

. .

. .

Fig. 7. Longitudinal data for two infants’ astigmatisms. The magnitudes of the cylinder errors as measured from photorefractive pictures are given together with indications

of the infants’ abilities to focus at 0.75 and 1.5m. 0: left eye. 0: right eye. n : consistent focusing at this distance. 0: no accurate focusing at this distance. q : inconsistent focussing at this distance. tism was taking place. At 6 wk with infant B only partially compromised values of the astigmatism seem to have been obtained as the value for the astigmatism is much lower than at other points on the graph.

Anisometropia

DISCUSSION

Of the 93 infants photorefracted,

only 2 showed a consistent spherical difference in focus of 0.5-I D between their two eyes. This result is not at variance with the incidence of anisometropia in the adult population. Of the 58 infants showing astigmatism of 0.75 D or greater, 6 met this criterion in one eye only and a further 4 showed a difference of more than 0.75 D astigmatism between the eyes. Longitudinal

A

1.0.o

By any of these criteria,

showed a small error on some pictures at one or other camera distance.

Infant l

2.0.

at 150 cm than at

observed. indicating that these infants were capable of taking up this accommodative state. All infants who could focus at 15Ocn-1 could also focus on targets closer than this distance although a very small number could not focus closer than 75 cm. None of our sample over 6mth of age failed to meet our criterion of good focus at both distances. A large percentage of our infants were astigmatic (Howland et al.. 1978) and could not focus in both meridians simultaneously. For some astigmatic infants some compromising was seen where both meridians

1327

data

Two infants were photorefracted on a number of occasions from birth throughout the first year of their lives. Both were astigmatic. A plot of the highest value for a minimal estimate in astigmatism in each session is plotted for each infant as a function of age in Fig. 7. The infant’s ability to focus at 75 cm and 150 cm in one axis is also shown on the same figure using criterion A. Infant A showed good accommodation at 75 cm from birth and accommodated over the entire range from 2 mth onwards. Infant B showed incopsistent accommodation over the first months, but by 6 wk accommodated at 75 cm, and by 4 mth accommodated over the entire range. Both infants show a decline in the highest minimum astigmatism over the time period tested. Both infants appeared astigmatic at each session they were tested. However, smaller values of the astigmatism were recorded in all sessions suggesting that some compromising of the astigma-

Accommodatice

ability

Our data indicate that, by the age of 6mth. all of our infant subjects could adjust their accommodation quite accurately over the full range, and that over 50% could do so by 2-3mth. (Because of the prevalence of astigmatism, this does not necessarily imply that the image was well focused in all cases.) From birth to 2 mth, accommodative ability improves, with a greater proportion of infants at each age showing accurate accommodation at relatively near (75 cm) than at far (150cm) distances. The general trend of these results is in agreement with the existing retinoscopic studies of infant accommodation (Haynes et al., 1965; Banks, 1978). However. two significant differences should be noted. First, we found that most I-2mth olds, and about half our neonates. could accommodate at 75cm within our criterion. This is a greater distance than would be implied by the data of Haynes et al. for this age group. While the 1.2 D “dead zone” allows this amount of myopic error to occur within our criterion, this is not enough to account for the discrepancy. Their 1 mth olds showed a constant accommodation at about 20 cm. which is 3.7 D myopic with respect to 75 cm. The second difference is the occurrence of what we have termed “inconsistent accommodation” in the

132s

OLNERBRADDICK.

JASETTE ATKINSON.

JENSIFER FRENCH

younger age groups; a substantial fraction of the infants showed occasional instances of good accommodation at distances where they did not accommodate consistently. This implies that the accommodative errors. of these infants at least, were not due to accommodation being locked at some near distance such as 20 cm. Rather, the accommodative system had the physica capacity to vary focus over a range that in many cases could extend at least to 150cm. What the infants are apparentlv unable or unwilling to do consistently is to use th’ls potential accommodative range to bring the target into sharp focus. Why infants do not use their power of aecommodation appropriately. especiafly over relatively large distances. remains an open question, In the discussion of acuity below, we suggest that they may not have the relevant visual information to do so. It is also entirely possible that a more effective target could be devised for compelling the infants’ attention and controlling their accommodation; it should be remembered that, to avoid pupil constriction, the photorefractive testing. was conducted under conditions of low photopic illumination. In conducting experiments with infants it is generally found that the “attentional field”, i.e. the area around the infant within which the infant’s attention may be attracted, is restricted even if the retinal size of the target remains constant (McKenzie and Day, 1972. 1976: Day and McKenzie. 1977). It is possible that the unwillingness of our infants to accommodate on distant targets is an attentional limitation rather than a visual or accommodative Iimitation. Although attempts were made at all times to photorefract infants only in an alert and calm state. an effect of sitting in a dimly lit, quiet room, particularly for the younger infants. is to make them drop asleep. It is possible that at least part of the inconsistent accommodatjon shown by the neonates or 1 mth olds was due to changes of state causing loss of attention. lmplicarions for acuity

The improvement of accommodative performance occurs over age range (O-6 mth) which shows a striking increase in behaviorally and eiectrophysiologicaily measured acuity. However. quantitative examination shows that the improvement in acuity cannot be ascribed to the optical improvement of the retinal image produced by accurate accommodation. First, it should be noted that most studies of infant acuity have been performed at rather near stimulus distances (the 40cm used by Atkinson et al., 1977, is typical), within the range of accurate accommodation for most I mth and older infants on the present data. Secondly. we niay estimate the effect of errors of focus on the spatiai frequencies present in the retinal image. The modulation transfer function of a defocused lens is given to a good approximation by the function from geometric optics given in Table 2. This function shows a number of zero-crossings with lobes whose magnitudes decrease with increasing spatial frequency. It is thus somewhat arbitrary to select an upper cutoff spatial frequency for a given degree of defocus; but a reasonable and convenient point is the first zero. No higher spatial frequency is transmitted with a contrast greater than 13Y&so given the contrast sensitivity of young infants (Atkinson et a[.,

and

HOWRD

C. HOWL.OD

Table 7. Calculated cut-off spatial frequency ICdeg) Pupil diameter (mm1

1D

1

5.3

’ 7

1.8

6 s

3.6 2.7

;:Y 1.3

1.1 0.9

Dioprric defocus 2D 3D

-1D 1.3 0.9 0.7

MTF of defocused lens = !J,(x);x where J, is the first order Bessel function. I = Zd(.Vcl)J d = defocus in mm’ ‘VA = numerical aperture = pupil radius:focal length, and f= spatial frequency (c mm). Cutoff taken as first zero oi

this function. for which x = 3.83.

1977: Banks and Salapatek, 1978). it is unlikely that any higher spatial frequencies can be detected. Table 2 gives the results of calculating this cutoff frequent! for various values or pupil size and dioptric defocus. Acuity values for I mth olds are typically in the region of I cideg (Atkinson ef al.. 1977: Dobson and Teller, 1975). The table shows that defocus will onI> be a significant constraint on acuities in this region for defocus of 3 D or greater combined with pupil sizes of over 6mm. Infants of this age rarely had pupils of this size in our tests, and neither our data nor that of Haynes er al. (1965) give any reason to suppose that they would .be accommodated 3 D or more away from a 40cm target distance. The acuitics of 2-5 c/deg typically found for 2-3 mth olds could be limited by dioptric errors of i-2 D and the norma range of pupil sizes; however, the accommodatj~e performance at this age again gives no reason to expect spherical errors of this size at the target distances used. Paradoxically, the cases where optical limits on acuity are most likely to have an effect are not the young infants where accommodation and acuity are relatively poor, but the older infants where they are relatively good. This is because astigmatic errors of 1-3 D are common in this age range. Such errors would have a detectable effect on image quality in one meridian for an infant with, say, a 6 mm pupil and an acuity of Zcideg or better. For the grating targets used in acuity studies, one might expect that the grating orientation would be brought into good focus where possible; but where one axis is myopic it ma> not always be possible, and where orientations besides the grating are present in the field of view it may not always occur. A preferential looking experiment on some of the subjects in our sample (Atkinson and French, 1979) has shown that their astigmatisms did indeed have a visual effect. In general then. our results imply that the improvement of infant acuity from O-6 mth is a result of the development of the neural structures that process the retinal image, rather than of the optical quality of the retinal image itself. It is entirely possible that the development of accommodative ability over this period is a consequence of the improvement in acuity, rather than cite versa. The accurate control of accommodation implies the ability to detect image defocus, so that the accommodative adjustment which minimizes defocus may be made, If. due to immaturity, the visual pathway does not transmit high spatial frequencies. this information is not available to detect image

1329

A photorefractive study of infant accommodation

defocus. A similar prop04 has been made by Owens and Held (in press) and Banks (1979). The occurrence of inconsistent accommodation. in which accommodation is apparently varying in a way that is not under the control of the target. is consistent with this suggestion. However, it should be noted that there is evidence that in adults. accommodative control is more sensitive to the contrast of intermediate spatial frequencies than to that of frequencies near the acuity limit (Owens, 1977). This does not necessarily invalidate the argument, but it does mean that, to support it fully, the analysis would have to be conducted in terms of the infant’s ability to detect contrast changes over a wide range of spatial frequencies. . Asrig0iarism The prevalence of significant astigmatism in infants aged O-l yr invites speculation as to its effects, its origin and its subsequent disappearance. The relation of this astigmatism to the development of visual sensitivity to different orientations has already been discussed by Howland et al. (1978) and by Mohindra et al. (1978). Most astigmatism in adults is due to differential cornea1 curvature in different directions, rather than to any anisotropy in the lens. Whether this is true also of our infantile astigmatism could best be resolved by keratoscopic measurements of cornea1 curvature, coupled with refraction of the same infants. If such measurements showed cornea1 astigmatism, it would suggest that a temporary anisotropic growth progress, or possibly a vulnerability to mechanical deformation, was responsible. The question remains why the astigmatism mostly disappears by later childhood (Blum et al., 1959). It is possible that the growth of the eye is programmed for a symmetrical goal, but that at an intermediate stage growth in different meridia is out of step. An alternative, and provocative, possibility is that isotropy is the usual result because the growth of the cornea is actually under the control of feedback from the quality or other parameters of the retinal image. While it is unclear what the route of such feedback might be, it is also a possible explanation of the findings of Raviola and Wiesel (1978) that deprivation of pattern vision can induce myopia in the eyes of infant monkeys. Implications for visual screening of infants

This study shows that photorefraction is a feasible, rapid, and safe method for the assessment of refractive state in infants of all ages, and suggests that it could be of value for the early detection of infants requiring refractive correction. Photorefraction very readily detects astigmatism; however, the present data show that quite large astigmatism is commonplace among infants in the tirst year, and so presumably no correction of this grow is required. Very large astigmatisms detected by photorefraction in the first year should be followed up, and photorefraction would also be appropriate for the detection of astigmatism in later years when its incidence is much reduced (Mohindra er al., 1978b). Anisometropia is also immediately apparent from the comparison of the two eyes’ photorefractive images. In view of its part in the aetiology of amblyopia

and strabismus, the early detection and correction of anisometropia is important. Our results indicate that the nomal infant can accommodate accurately at 75 and 150 cm by the age of 6-8 mth. An inability to do so could be detected by photorefraction around this age and would probably indicate marked myopia. Hypennetropia is less easily detected, since any but a very severe hypermetrope would have sufficient range of accommodation to focus at these camera distances. Infant hypermetropia is believed to be an important cause of esotropic strabismus, so its detection would be desirable. Research is in progress at present to see whether it might be achieved by photorefraction of infants wearing a negative spectacle lens. CONCLUSlONS 1. Infants of 6 mth and over normally show consistent and accurate accommodation over a working range extending out to at least 150 cm. Most infants of 1 mth and over, and many neonates, can accommodate at 75 cm and closer. 2. Accommodative errors by infants under 6mth are insufficient to account for their reported relatively low acuity. 3. The occurrence of occasional but inconsistent accurate accommodation at 75 and 150cm in young infants suggests that they do not lack the capability to accommodate at these distances. but cannot or will not control their accommodation appropriately. This may be a consequence of poor acuity or of the infant’s limited attentional field. 4. Marked astigmatism is widespread in the first year of life, and its visual effects can be demonstrated. Its origin and long-term consequences, if any, are not

yet known. 5. Photorefraction may serve as an effective technique for the refractive screening of infants in the future. Acknowledgements-Photorefractive attachments used in this study were constructed by Bradford Howland and by Dr R. Willstrop and Mr J. Cullum. We also thank Bradford Howland for invaluable discussion. We are grateful for the cooperation of Dr N. R. C. Roberton and the staff of the Cambridge Maternity Hospital. and to our volunteer parents and infants. This work was supported by a project grant from the Medical Research Council of Great Britain. We thank Professor 0. L. Zangwill for provision of facilities for infant research in the Psychological Laboratory. Howard C. Howland was a guest in the laboratory of Dr F. W. Campbell, Physiological Laboratory. Cambridge, during the period of this research. We are indebted to Joanne Ballarino and Dana Wong for technical assistance with the photorefraction of the adults and to Monica Howland for assistance with the diagrams and figures. REFERENCES Atkinson J., Braddick 0. and Moar K. (1977) Development of contrast sensitivity over the first 3 months of life in the human infant. Vision Res. 17, 1037-1044. Atkinson J. and French J. (1979) Astigmatism and orientation preference in human infants. This issue, p. 1315. Banks M. S. (1978) Visual accommodation in human infants (abstract). Meering of the Association for Research in Vision and Ophthalmology. Inc. (ARVO), Sarasota. Florida.

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