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Ophthal. Physiol. Opt.

2008 28: 115126

Gender differences in early accommodation


and vergence development
Anna M. Horwood and Patricia M. Riddell
Infant Vision Laboratory, School of Psychology & Clinical Language Sciences, University of Reading,
Earley Gate, Reading, UK

Abstract
A remote haploscopic photorefractor was used to assess objective binocular vergence and
accommodation responses in 157 full-term healthy infants aged 16 months while fixating a brightly
coloured target moving between fixation distances at 2, 1, 0.5 and 0.33 m. Vergence and
accommodation response gain matured rapidly from flat neonatal responses at an intercept of
approximately 2 dioptres (D) for accommodation and 2.5 metre angles(MA) for vergence, reaching
adult-like values at 4 months. Vergence gain was marginally higher in females (p = 0.064), but
accommodation gain (p = 0.034) was higher and accommodative intercept closer to zero (p = 0.004)
in males in the first 3 months as they relaxed accommodation more appropriately for distant targets.
More females showed flat accommodation responses (p = 0.029). More males behaved hyperme-
tropically in the first two months of life, but when these hypermetropic infants were excluded from the
analysis, the gender difference remained. Gender differences disappeared after three months. Data
showed variable responses and infants could behave appropriately and simultaneously on both,
neither or only one measure at all ages. If accommodation was appropriate (gain between 0.7 and
1.3; r2 > 0.7) but vergence was not, males over- and under-converged equally, while the females
who accommodated appropriately were more likely to overconverge (p = 0.008). The apparent
earlier maturity of the male accommodative responses may be due to refractive error differences but
could also reflect gender-specific male preference for blur cues while females show earlier
preference for disparity, which may underpin the earlier emerging, disparity dependent, stereopsis
and full vergence found in females in other studies.

Keywords: accommodation, development, gender, infant, vergence

development (Held et al., 1980; Birch et al., 1982) are


Introduction
all reported to develop earlier during infancy in females.
Gender differences are rarely the focus of developmental These differences appear to be most marked between
vision research and in the majority of the developmental approximately 10 and 20 weeks. For acuity, vernier
literature, it is difcult to ascertain if gender was acuity develops earlier in females (Held et al., 1984), and
ignored, or considered and found to be insignicant, VEP acuity has been reported to be poorer in 16-week-
and so not reported. Differences have been reported, old males (Makrides et al., 2001) but grating acuity does
however, in many aspects of early vision. In terms of not appear to show a developmental gender difference
binocularity, preference for binocularly fusible targets, during the rst year of life (Held et al., 1996).
full convergence (Held et al., 1996) and stereopsis The available evidence is clearer for earlier female
development in processes that require disparity detec-
tion, such as vergence, preference for fusible targets and
Received: 26 September 2007 stereopsis, while being more equivocal for blur detection
Revised form: 28 November, 4 January 2008 tasks such as acuity measures. Broadly stable ocular
Accepted: 12 January 2008 alignment is likely to be necessary for emergence of
Correspondence and reprint requests to: Anna M. Horwood.
stereopsis and accurate vergence at 1216 weeks, and
Tel.: +44 0118 378523; Fax: +44 0118 3786715. has been shown to be present from the rst days,
E-mail address: a.m.horwood@reading.ac.uk provided allowance is made for the large angle lambdas

2008 The Authors. Journal compilation 2008 The College of Optometrists doi: 10.1111/j.1475-1313.2008.00547.x
116 Ophthal. Physiol. Opt. 2008 28: No. 2

of infancy (Horwood, 1993, 2003b; Hainline and Rid- Ciuffreda, 1999; Goldschmidt, 2003). For instance,
dell, 1995, 1996). In a period when acuity is poor myopia has been reported to be more common in
(Gwiazda et al., 1980), and refractive errors are com- school age females by some authors (Dandona et al.,
mon and change rapidly (Gwiazda et al., 1980, 1993; 2002; Morgan et al., 2006), but not others (Gwiazda
Gwiazda and Thorn, 1998), however, blur may be a less et al., 2002; Zadnik et al., 2003; Lam et al., 2004).
reliable visual cue. Wesson et al. (1990) failed to nd refractive gender
The development of accommodation responses in differences in a group of younger children between
infants has been shown to progress from relatively xed 3 months and 9 years. Hypermetropia and astigmatism
near focus in neonates to adult-like response slopes by were found to be less common in 67 year old males
34 months (Haynes et al., 1965; Braddick et al., 1979; than females by Chen et al. (1996). Krause et al. (1982)
Banks, 1980; Brookman, 1983; Howland et al., 1987; found hypermetropia and myopia to be less common in
Currie and Manny, 1997). Motor accommodation 14-year-old males but more severe when it did occur.
responses have recently been shown to mature earlier Zadnik et al. (2003), however, found that school-aged
than sensory aspects of the visual system (Tondel and females have steeper corneas. Similarly, anisometropia
Candy, 2007) and can be adult-like by 8 weeks of age, (Pointer and Gilmartin, 2004; Garcia et al., 2005) and
well before the majority of emmetropisation has taken intermittent exotropia have been reported to be more
place (Mohindra and Held, 1981; Gwiazda et al., 1984, common in school age females (Nusz et al., 2005).
1993; Ehrlich et al., 1997), but gender differences have Accommodation and convergence anomalies have not
not been reported so far. been reported to show a gender difference (Rouse et al.,
Our laboratory is studying the precursors to the 1999), but are commonly found in conditions such as
development of mature vergence and accommodation in dyslexia, which is more frequently reported in boys
terms of responses to different near cues. In view of the (Evans et al., 1994). Amblyopia does not appear to
reported gender differences in the emergence of the show a gender difference (Attebo et al., 1998).
disparity-dependent aspects of binocular vision, we In this study, we found a previously unreported
looked for gender differences in the weeks preceding gender difference in the very early development of
the emergence of these processes as part of our ocular accommodation, and to a lesser extent ocular
preliminary data analysis of a longitudinal study of convergence, which we relate to current literature on the
infant accommodation and vergence development. development of vergence and accommodation and
Although gender differences were not the main motiva- which highlights gender as an issue that should be
tion for the study, we predicted that the earlier sensory considered in early developmental research.
development of retinal disparity detection found by
others in females could be underpinned by a similar
Methods
earlier maturation in adult-like vergence control.
Early gender differences are less likely to be due to Sixty-seven female and 90 male full-term, healthy infants
environmental inuences that are thought to inuence attended the Infant Vision Lab as part of a large
later refractive development (Adams and McBrien, longitudinal study of the development of vergence and
1992; Troilo, 1992; Zylbermann et al., 1993; Simensen accommodation between the rst and sixth months of
and Thorud, 1994; Goldschmidt, 2003), but could form life [see Table 1, which details the number of infants
the foundation for later visual development. They might providing reliable data (in terms of attention and
also inuence the prevalence of later-developing ocular photograph quality) at each age group]. Infants
conditions such as clinically signicant refractive error, attended for a mean of 3.12 visits with no difference
strabismus, accommodative, or convergence anomalies, between the number of visits for male and female infants
in which abnormalities of the typically developing [t (157) = 0.51, p = 0.62]. Here we report the infants at
vergence, accommodation, or binocular vision mecha- monthly intervals up to 6 months. Ethical approval was
nisms are implicated. Conversely, innate or genetically obtained from the University of Reading Research
determined gender differences may be compensated by
later adaptive mechanisms, such as emmetropisation
and vergence adaptation, and so disappear during Table 1. Numbers of infants in each age group who provided
development. reliable data in terms of attention and photograph quality
While many studies have looked for gender differ-
Age (months)
ences in older children, the evidence is sparse and
equivocal. What evidence there is could equally support 1 2 3 4 5 6
environmental differences or genetic factors (Parssinen
Males (n) 18 52 66 57 40 33
et al., 1989; Adams and McBrien, 1992; Zylbermann
Females (n) 13 32 42 35 23 30
et al., 1993; Simensen and Thorud, 1994; Hung and

2008 The Authors. Journal compilation 2008 The College of Optometrists


Gender differences in vergence and accommodation: A. M. Horwood and P. M. Riddell 117

Ethics Committee and informed consent was obtained (Choi et al., 2000; Gwiazda and Weber, 2002; Allen
according to the Declaration of Helsinki. et al., 2003) so two independent scorers made a
Accommodation and convergence were assessed using judgement of the position of crescent border. Corre-
a remote haploscopic off-axis photorefractor (RHP) lation between scorers was r2 = 0.9946 and Bland
reported in detail elsewhere (Horwood et al., 2001; Altman analysis (Bland and Altman, 1986, 1999)
Turner et al., 2002) and similar to that described by provided limits of agreement (around the mean
Abramov et al. (1990). This photographed the infants inter-scorer difference of 0.0063 D) of 0.19 D. All
eyes while they xated a monitor displaying a brightly measurements for photorefraction and calibration
coloured picture of a clown with gross and ne details were taken in the vertical meridian. While we accept
(subtending 2.8 4.2 at 2 m). Photographs were taken that there is an increased prevalence of astigmatism in
with the infant xating the target on a monitor which infants and we were unable to calibrate the measure-
moved along a motorised beam to positions at 2, 1, 0.5 ments for each infant as suggested by Blade and Candy
and 0.33 m from the infants eyes, presented in a pseudo (2006), our data primarily report change in response
random order starting at 0.33 m. As we needed good between target distances within individuals rather
photographs at each of four xation distances and some than absolute refractive error. Even if a measure of
of the infants were extremely young, only one photo- absolute refraction between infants is subject to
graph was taken at each xation distance. We were some variability, the response at each xation distance
therefore unable to obtain repeatability data. We did, within an individual infant should be changed by the
however, make great efforts to ensure that the infants same constant and so response slopes should not be
were in a calm alert state during testing and photo- inuenced by this increased variance (provided it is
graphs were only taken when the infant was observed by additive). From our original calibrations, we have no
the examiner (on a separate infra-red monitor) to be evidence that the constant was multiplicative rather
attending to the target. A recent study has suggested than additive.
that infants from 8 weeks of age have a response latency Graphs were plotted of the simultaneous vergence and
of <1 s (Tondel et al., 2005). This period was always accommodation responses for each infant against target
exceeded in our laboratory by the time it took for the demand (Figure 1). Vergence data were converted to
examiner to decide attention was adequate and for the metre angles (MA), taking into account inter-pupillary
photograph to be taken. distance (IPD) at each visit, and in dioptres (D) for
Photorefraction photographs of the eyes were taken accommodation, so that slopes could be plotted on the
via a beam splitter so that the photorefracting camera
and the target appeared directly in front of the infant,
while being on separate visual pathways. Ocular ver-
gence angle was calculated in metre angles from
changes in position of the rst Purkinje image in
relation to the pupil centre on each photograph, with
an age-appropriate correction made for angle lambda
(Riddell et al., 1994)1. An adult control group xated a
series of ve targets at 5 horizontal intervals so that we
could assess gaze accuracy, which was 1.1 (Horwood
et al., 2001).
The accommodation (in dioptres) was calculated
from measurements of the size of retinal reex crescent
in the pupil. Accommodation responses were calibrated
using an adult control group where RHP responses
were compared with dynamic retinoscopy while the
participants xated the same target. The data were then
processed using neural network techniques to produce
a smooth two-dimensional surface that could be used
for all photorefraction data. Accuracy was 0.3 D
for accommodation data. Our study started before
the availability of more recent automated methods

1
Angle lambda is dened as the angle between the line of sight and the Figure 1. Actual data from an infant aged 17 weeks. Total vergence
pupillary axis. equals the sum of the two separate adduction measurements.

2008 The Authors. Journal compilation 2008 The College of Optometrists


118 Ophthal. Physiol. Opt. 2008 28: No. 2

same graph. Any obvious outlying points from a photographs because of poor cooperation or exclusion
monotonic response were excluded from the four data of outliers. If a photograph was excluded or missing, the
points tested [such as the intermittent large neonatal possible optimum range could vary between 1.5 D or
misalignments that occur in many infants (Horwood, MA (if the 3 D target was missing), 2.0 D or MA (if the
2003a; Horwood and Riddell, 2002; Horwood and 0.5 D target was missing), and 2.5 D or MA (if the 1 D
Williams, 2001), which were dened as more than or 2 D photograph was missing). There were no
two standard deviations of the total sample response signicant gender differences in the number of photo-
in excess of target demand, or more than two stan- graphs at each distance that were missing [v2 (2) = 1.84,
dard deviations more divergent than orthoposition]. p = 0.4], or in the mean optimum range possible [t
Because a pseudo-random order of testing was (561) = 1.3, p = 0.63], i.e. missing data were equally
used, where a near target was always preceded by a distributed between the genders. Infants around
more distant one or vice versa, any appropriate and 16 weeks were more intensely interested in the target
linear response slope was likely to indicate reliable than those both younger and older, and missing data
xation. points were evenly distributed between the older and
Vergence angle and accommodation from at least younger infants, i.e. more stable and appropriate
three of the four possible xation distances (and four responses in the older infants were not due to the
if available) were used to calculate slope, r2 and absence of data.
y-intercept of the line that best tted the data. Slope Responses are illustrated in Figure 2. Vergence slope
represents the gain of the response to target distance (Figure 2a) increased rapidly in the rst 4 months. A
and y-intercept reects an estimate of focus at innity. two-way between-groups overall ANOVA [F(11,431) =
A slope of 1.0 represents perfect response to target 4.429, p < 0.0001] with age and gender as factors
demand, while any slope of <1 can be produced by showed a highly signicant main effect of age
under-response for near and/or failure to relax at [F(5,431) = 7.841, p < 0.0001]. There was also a mar-
distance. A positive intercept represents overconver- ginal main effect of gender [F(1,431) = 1.206,
gence and overaccommodation at innity, while a p = 0.064] with females having slightly higher slopes
negative intercept represents negative accommodation, than males. There was no signicant interaction and
i.e. a hypermetropic crescent. As cycloplegic eyedrops post hoc t-tests did not show any individually signicant
were not used, this y-intercept gives an estimate of gender differences in any single month.
manifest refractive error, but can mask latent hyper- Similarly, vergence y-intercept, and r2-values (Fig-
metropia. A negative y-intercept according to our ure 2c,e) all showed signicant improvements with age,
analytical procedure represents a degree of hypermetro- although range (Figure 2g; difference between maximum
pia, but the absence of negative y-intercept may mean an and minimum response) did not change signicantly
infant is either truly not hypermetropic, or is over- across the ages tested. (y-intercept: overall
coming their hypermetropia appropriately by accom- F(5,431) = 3.998, p < 0.0001, main effect of age
modation. A positive y-intercept could reect true F(5,431) = 8.193, p < 0.0001, no main effect of gen-
myopic refractive error or xation proximal to innity. der; r2: overall F(11,431) = 6.641, p < 0.0001), main
Range of responses was taken as the difference between effect of age F(5,431) = 12.782, p < 0.0001, no main
the maximum and minimum responses found over the effect of gender; range: overall F(11,431) = 1.647,
four target distances. p = 0.083). Post hoc testing generally showed that the
Statistical analysis was performed using SPSS 14. Due greatest change occurred between months 2 and 4 (for
to increased variance in the younger groups, post hoc age effects see Appendix 1), with some reduction in
testing was carried out using the more conservative vergence and accommodation slope between months 4
GamesHowell procedure. It would have been prefera- and 6. In general, infants at four months were intensely
ble to do within groups analysis, but only a small engaged by the target, but by 6 months were more easily
number of subjects provided reliable data over the whole distractible and more difcult to test, as has been found
testing period. Although trends were very similar (and by others (Braddick and Atkinson, 1979; Hainline et al.,
indeed prompted us to re-visit our cross-sectional data), 1992; Atkinson, 2000).
the small numbers who provided a full set of longitu- The gender differences were signicant in the accom-
dinal data prevented us being able to detect the effect modative domain. As with vergence, there were signi-
statistically that we report here. cant main effects of age on all four measures
(Figure 2b,d,f,h; slope: F(11,431) = 6.797, p < 0.0001;
y-intercept: F(5,431) = 22.974, p < 0.0001; range:
Results
F(5,431) = 8.037, p < 0001; r2: F(5,431) = 11.597,
There were no signicant gender differences in the p < 0.0001, see Appendix 1). Gender differences were
number of infants who provided three rather than four signicant for both accommodative slope and y-inter-

2008 The Authors. Journal compilation 2008 The College of Optometrists


Gender differences in vergence and accommodation: A. M. Horwood and P. M. Riddell 119

(a) Vergence Slope (b) Accommodation Slope


1.2 1.2
1.0 1.0
0.8 0.8
0.6 0.6

Gain

Gain
0.4 Males 0.4
Males
0.2 Females 0.2
Females
0.0 0.0
0.2 0.2
0 2 4 6 8 0 2 4 6 8
Months Months

(c) Vergence intercept (d) Accommodation intercept


4.0 4.0
3.5 Males 3.5 Males
3.0
(*)
3.0
Intercept (MA)

Intercept (MA)
2.5 Females 2.5 Females
2.0 2.0
1.5 1.5 *
1.0 1.0
0.5 0.5
0.0 0.0
0.5 0.5
1.0 1.0
0 2 4 6 8 0 2 4 6 8
Months Months
(e) Vergence Rsq (f) Accommodation Rsq
1.0 1.0
0.9
0.8 0.8
0.7
0.6 0.6
2 0.5
r2 r
0.4 0.4
0.3 Males
Males 0.2
0.2
Females 0.1 Females
0.0 0.0
0 2 4 6 8 0 2 4 6 8
Months Months

(g) Vergence range (h) Accommodation range


4.0 4.0
3.5 3.5
3.0 3.0
Range (MA)

Range (D)

2.5 2.5
2.0 2.0
1.5 1.5
1.0 Males 1.0 Males
0.5 Females 0.5 Females
0.0 0.0
0 2 4 6 8 0 2 4 6 8
Months Months
Figure 2. Vergence (a, c, e, g) and accommodative (b, d, f, h) responses (SE) at each age group. Slope increases to near 1.0, y-intercept
reduces to near zero, Rsq increases and accommodative range increases with age. Gender differences are evident for accommodation slope
and intercept, with males showing more adult-like responses. There is a significant main effect of gender on accommodative slope and
y-intercept, and a marginal gender main effect on vergence slope. Post hoc significant gender differences (p < 0.05) marked *, marginal
difference marked (*) (p > 0.05 < 0.07).

cept (slope F(1,431) = 4.522, p = 0.034; y-intercept (32) = )1.93, p = 0.06]. The gender difference was,
F(1,431) = 8.337, p = 0.004) but not for range or r2. however, signicant in month 2 [t (82) = )2.047,
Girls showed atter accommodative slopes and higher p = 0.044]. The difference was not signicant at any
y-intercepts than the boys. Agegender interactions were other age tested.
not signicant. Accommodation response slope becomes steeper with
Post hoc t-testing of accommodative y-intercept age, as infants both increase accommodation for near
showed that, although the mean difference between targets, and, more particularly, relax accommodation at
males and females for the 1 month infants was greater distance. The steeper slopes in males may be due to
than at other ages, reduced power as a result of the males making more appropriate responses to near or
smaller number of infants tested resulted in an distant targets, males inappropriately overaccommodat-
only marginally signicant difference at month 1 [t ing at near or females overaccommodating at distance.

2008 The Authors. Journal compilation 2008 The College of Optometrists


120 Ophthal. Physiol. Opt. 2008 28: No. 2

The mean data from the female infants made the


accommodative slope in Figure 3(a) appear nonlinear,
perhaps implying that females are less sensitive to subtle
target differences between 0.5 and 1 D. We considered
whether tting a nonlinear function to individuals plots
would better reect the data, or whether more female
infants showed an all or nothing (S shaped curve;
Hainline et al., 1992) response, but on examination of
individual responses it was clear that trying to t any
more complex curves would be spurious in view of the
limited amount of data points tested and the variability
of responses. There were no gender differences in the
number of all or nothing responses.
The y-intercept (estimate of focus at innity) repre-
sents an estimate of manifest refractive error. While this
cannot be compared with cycloplegic refraction and may
mask hypermetropia controlled by appropriate accom-
modation, any hypermetropic crescent found during
testing indicates a degree of hypermetropia at some
time, which may be useful in identifying hypermetropic
infants. Although, over all age groups, there were no
signicant differences in the number of infants who
showed hypermetropic y-intercepts, Table 2 shows that,
in the rst 3 months, many more males showed hyper-
metropic y-intercepts than females (v2 = 5.7, d.f. = 1,
p = 0.017). In the rst two months of life, indeed, the
gender difference is marked (v2 = 8.9, d.f. = 1,
p = 0.003) while after three months of age these
differences disappear (v2 = 0.076, d.f. = 1, p = 0.78).
As hypermetropic infants might produce steeper slopes
if over-relaxing accommodation for distant (and smal-
ler, perhaps less engaging) targets but accommodating
appropriately for near, a larger number of hypermetro-
pic males may have caused an apparent difference in the
Figure 3. Accommodation responses (SE) at each fixation dis-
mean accommodation responses, so we excluded all the
tance at 2 months of age. (a) responses of whole group. (b) data from any infant who had demonstrated a hyper-
responses of infants who had never shown a hypermetropic metropic crescent at any time in the rst 4 months of life
response at any age, showing greater gender difference. Post hoc and re-examined the data from the 31 females and 33
significant gender differences are marked * (p < 0.05), and marginal males remaining, concentrating on actual responses to
differences are marked (*) (p > 0.05 < 0.07). the different target demands rather than the y-inter-
cepts. While the gender difference in accommodative
response at 0.5 m at 2 months was only marginally
Figure 3a shows that at 2 months of age males are signicant when the infants who showed hypermetropic
making marginally more appropriate distance responses crescents were included, despite smaller numbers,
than the females [t (65.98) = )1.705, p = 0.078] while the difference was greater if these hypermetropic
near responses are similar. infants were excluded [t (28.53) = )2.33, p = 0.027;

Table 2. Numbers of infants (and percentages of numbers tested in each category) at each age group who showed hypermetropic y-intercepts
(top row) and hypermetropic y-intercepts >1.00 D (bottom row)
Age (months) 1 2 3 4 5 6

m f m f m f m f m f m f

Any hypermetropic intercept 3 (16) 0 (0) 22 (42) 5 (16) 43 (65) 26 (47) 41 (71) 24 (68) 25 (63) 15 (65) 18 (55) 20 (66)
Hypermetropic intercept >1.0 1 (6) 0 (0) 10 (19) 1 (3) 15 (23) 8 (19) 14 (25) 11 (31) 10 (25) 5 (22) 8 (24) 4 (13)

2008 The Authors. Journal compilation 2008 The College of Optometrists


Gender differences in vergence and accommodation: A. M. Horwood and P. M. Riddell 121

Figure 3b]. Males continued to show more accurate


accommodation to the distant target while females
over-accommodated to it.
The data from individual participants were variable,
as might be expected at this age, but also reects the
variability that we found at all ages in this naturalistic
setting. Positive correlation between vergence and
accommodation responses was statistically signicant
at each month, but was generally not strong (r-values
of between 0.33 and 0.49, with no developmental
trends) The r2-values of the slopes, however, (rather
than accommodation vs vergence responses) of approx-
imately 0.5 even in the youngest infants indicate largely
linear responses to demand even when slopes were
low and accommodation was not necessarily doing
the same as vergence. It was noticeable that for many
testing sessions, vergence responses were reliably better
than accommodation or vice versa, despite responses
for both measures being taken from the same photo-
graphs and the data recording session itself being
reliable in terms of attention. Thus, infants could show
accurate vergence, accommodation, both, or neither, at
each testing. Signicantly more females showed at
accommodation slopes (slope of <0.3 and y-intercept
>1.5 D) in the rst 3 months of life than males
(v2 = 4.76, p = 0.029).
We classied the good responses as those showing a
slope of between 0.7 and 1.3 with an r2 of at least 0.7.
Not having a good response does not mean that the Figure 4. Percentages of infants in each age group showing good
infant was behaving unreliably, but only with gain responses (slope between 0.7 and 1.3 and r2 > 0.7) to vergence,
outside these limits. Overall, from the fourth month accommodation or both.
onwards, approximately 50% of infants showed good
responses on only one of the two measures, and this nostic determinants of VEP acuity. To check whether
proportion did not change with increasing age (Fig- birth weight was an important factor in our study, we
ure 4). reanalysed the data using an ANCOVA, with birth weight
We looked at the relationship between vergence and as a covariate, but this did not change the results.
accommodation in males and females. If a male showed
good accommodation, but not good vergence, the
Discussion
vergence was equally likely to be an underconvergence
or overconvergence. In comparison, 61.9% of females Gender differences are rarely the focus of ocular
with good accommodation responses showed higher developmental literature and, as in our report, may
vergence slopes (v2 = 7.062, p = 0.008), i.e. girls not have been the main motivation of studies where such
tended to overconverge when they accommodated differences have been found. There is, however, a small
appropriately. When vergence was good but accom- body of literature on gender differences in early devel-
modation inaccurate there were no signicant gender opment (Held et al., 1980, 1984, 1996; Birch et al., 1982;
differences. Makrides et al., 2001), to which this study adds, which
As male birth weight is generally higher than that of suggests that gender is a variable that should be
females (Scott et al., 1982), this apparent gender differ- considered more systematically.
ence might be accounted for by differences in birth The overall developmental ndings presented here are
weight (and therefore possibly associated axial length or similar to other published studies (Brookman, 1983;
neural development) rather than gender. Indeed, Mak- Hainline et al., 1992; Hainline and Riddell, 1996; Currie
rides et al. (2001) showed that, at 16 weeks of age, and Manny, 1997). While Hainline and Riddell (1996)
higher birth weight was associated with better VEP reported on a larger group, the group size reported here
acuity, while male gender was associated with poorer compares well with other studies (Brookman, 1983;
acuity in a dietary intervention trial looking at prog- Howland et al., 1987; Currie and Manny, 1997). Our

2008 The Authors. Journal compilation 2008 The College of Optometrists


122 Ophthal. Physiol. Opt. 2008 28: No. 2

infants progressed from at response slopes and rela- Male infants have steeper slopes, larger ranges and
tively xed y-intercepts of approximately 2 D for lower (less myopic/more hypermetropic) y-intercepts
accommodation and 2.5 MA for vergence, to more than female infants who at rst show atter responses
adult-like responses by 4 months. It is possible that the (low range, slope and more myopic distance focus). This
33 cm starting point may cause early at-lining result- appears to conict with the other visual developmental
ing from the distance at which the rst target appeared. literature (Held et al., 1980, 1984, 1996; Birch et al.,
While this is possible, our ndings are very similar to 1982; Makrides et al., 2001), which suggests that females
reports from other laboratories using different methods are generally developmentally ahead of males, and
and presentation order (Haynes et al., 1965; Brookman, importantly in this case, earlier to demonstrate both
1983; Aslin et al., 1990; Currie and Manny, 1997). Some sensory and motor aspects of binocular vision (Held
infants needed to be distracted or comforted in between et al., 1980, 1996; Birch et al., 1982). The gender
photographs in the testing sequence, so that the starting differences we found occur in the rst 2 months of life,
point for the resumed testing was not the 3 D target. before the age that differences in vernier and stereoa-
There was no difference in the intercept of the at cuity are reported to be maximal (Held et al., 1996),
responses from these infants. thus the earlier differences we report here may underpin
The large variance in response (see error bars in these processes.
Figure 2), particularly for slope and y-intercept of both Adult studies have demonstrated links between ver-
vergence and accommodation, reect the wide response gence and accommodation (Fincham and Walton, 1957;
variability found in all age groups, but particularly in Flom, 1960) and these have been extensively researched
the youngest infants. over the years (e.g.Ciuffreda et al., 1997; Schor, 1986b).
The apparent steady improvement in mean gain for If vergence and accommodation are linked early in
both accommodation and convergence is somewhat development, we would expect the vergence and accom-
misleading as this combines the results from many modation responses to be similar. Many infants showed
infants who showed at response slopes in their rst at accommodative responses but appropriate vergence
weeks then rapidly changed to adult-like responses by (or vice versa) at the same visit, despite estimates of both
the next testing session, with those who truly made a measures being taken from the same photographs. The
gradual developmental change. Vergence, in particular, fact that our data suggest that for many infants
is extremely variable in early infancy. Although we accommodation and vergence can act independently at
excluded very large neonatal misalignments (Horwood the same point in time, and that greater gender
and Riddell, 2002; Horwood, 2003a), which represent differences were found in accommodation than vergence
the extremes of the distribution, early vergence is still argues against any early strong linkage between the two
much more active than accommodation. Some infants systems. Since we report binocular data in this study,
showed appropriate vergence even on their rst visit, however, we are unable to make any further inferences
while others showed at responses, and most infants had about their relationship.
at accommodation at rst. This early variability also In terms of style of response, if infants accommo-
accounts for the lack of increase in vergence range with dated appropriately, females were more likely to show
age (as might be expected as responses become more overconvergence rather than underconvergence, while
target-appropriate). Greater range in the youngest males who accommodated appropriately were equally
infants was due to neonatal inter-individual variability, likely to show under- or over-convergence. Females
but in the older infants was due to appropriate near to were more likely to have at accommodation slopes.
distance response. The larger number of females who had vergence slopes
The only gender difference in the vergence domain close to and above 1.0 has the effect of raising their
was the marginally signicant lower slopes for the males, overall mean vergence slope in the rst months and may
suggesting they might have atter vergence responses. account for the marginal vergence slope effect.
The increased variance in the early vergence responses There are three possible explanations for our ndings.
reduced the power of the analysis, and thus the ability to Firstly, it may be true that males generally have an
demonstrate a signicant effect, but we cannot exclude accommodative response that is more adult-like than
the hypothesis that males could be slightly less female infants, or it might be that the proportion of
responsive to disparity than the females. This would males that show early maturation of accommodation
support the hypothesis that the early disparity difference responses is greater than in females. Figure 3 shows that
in females is underpinned by an earlier motor at two months males are making more appropriate
advantage. responses to distant targets. This could be explained by
The gender difference in the accommodation data, better visual acuity development and therefore ability to
however, is more robust, but in this case it is the males resolve the distant target, but evidence in the literature is
who appear to behave in the more adult-like manner. sparse, and what exists suggests that some (Held et al.,

2008 The Authors. Journal compilation 2008 The College of Optometrists


Gender differences in vergence and accommodation: A. M. Horwood and P. M. Riddell 123

1984; Makrides et al., 2001), if not all (Held et al., by gender differences in the type or amount of
1996), aspects of acuity are worse in males. Alternatively astigmatism that is known to occur in infants, although
it may reect gender differences in motor development such differences have not been reported in the literature
of the accommodation mechanism. Males have been (Gwiazda et al., 1984; Ehrlich et al., 1997).
found to precede females in other motor control A third hypothesis is that females use disparity cues
domains (Pomerleau et al., 1992; Piek et al., 2002). [or at this age, bifoveal xation (Hainline and Riddell,
A second explanation may be to do with differences in 1996)] in preference to blur, thus producing atter
refractive error, which we only assessed by non-cyclo- accommodation slopes, while males use blur more than
plegic methods and in one meridian, so cannot fully disparity. Previous studies have shown gender differ-
explore. (We were unable to use cycloplegia as these ences in stereopsis and full convergence (Held et al.,
infants were part of a large longitudinal study where we 1980, 1996; Birch et al., 1982), processes which depend
needed to retain maximum co-operation for repeated on disparity (rather than blur) detection. If disparity
testing). A hypermetropic infant would have to accom- cues and the responses to them are carrying more weight
modate more to clear a near target, but may relax than blur cues in females, it may explain the earlier
accommodation to hypermetropic focus for a distant, emergence of the disparity-dependent full vergence
smaller and therefore possibly less stimulating target. In (Held et al., 1996) and stereopsis (Held et al., 1980;
this case a hypermetropic infant would have a steeper Birch et al., 1982).
response slope (accurate for near and hypermetropic for We were unable to explore accommodative conver-
distance). A steeper response slope might also have the gence/accommodation(AC/A) and vergence accommo-
effect of producing a lower extrapolated y-intercept. dation/vergence (CA/C) relationships in this closed loop
Males, therefore, might be genuinely more hypermetro- study, but it might be predicted that if females prefer to
pic than girls, or the refractive errors could be equally use disparity and males prefer blur, the CA/C ratio
distributed across gender, but the female infants pro- might be higher in females and the AC/A ratio higher in
duce greater accommodative effort to overcome their males. Further studies are addressing this question.
refractive error at all distances. Further examination of Accommodation has been reported to be present in
the data showed that there was indeed a larger number some infants from 8 weeks (Tondel and Candy, 2007).
of males who produced a y-intercept of <0 (i.e. We report data from infants younger than those tested
hypermetropic), but this was true only in the rst by Tondel and Candy, who do not report gender
2 months. This suggests that males could either be truly differences in their slightly older group. Experience from
more hypermetropic than the girls at this age, or that the our lab (Turner et al., 2002) and others (Hainline et al.,
males of this age were not controlling their hyperme- 1992) suggests that infants start to use accommodation
tropia in the distance. From the third month of age relatively suddenly. If males respond preferentially to
onwards, approximately 65% of infants of both genders blur in their rst weeks, they may switch on to
had a hypermetropic y-intercept, as would be expected appropriate accommodation earlier than the females.
from the cycloplegic studies documenting hypermetro- While VEP (Makrides et al., 2001) and vernier acuity
pia in early childhood (for review see Thorn et al. 1996). (Held et al., 1984) have been reported to be poorer in
Thus, the early gender difference disappears, perhaps as males, grating acuity has not (Held et al., 1996), so
male infants begin to accommodate to overcome their resolution differences should not limit responses.
hypermetropia in the distance as well as for near. While collecting data from our laboratory (Turner
If the gender difference was due to a higher number of et al., 2002), it was clear that removing disparity cues
males being hypermetropic, then the gender difference in disrupts accommodation much more in some individu-
accommodation slope should reduce when hyperopes are als than others, and the clinical literature (Kushner,
excluded. In fact, the gender difference was even more 1988; Ansons et al., 2001; Grifn and Grisham, 2002)
marked (Figure 3) and showed that the difference in stresses that responses to therapies such as prisms and
slopes results from the males focusing more accurately at lenses can be idiosyncratic. The characteristics of
distance than the females, rather than resulting from individual idiosyncrasies of near cue use are rarely
differences in hypermetropic manifest refractive error. reported, but may be important in both development,
This argues against a true refractive error difference. and clinical diagnosis and decision-making, as stressed
No gender differences have been reported in published throughout clinical texts (Kushner et al., 1993; Kushner,
infant cycloplegic refraction data and our manifest 1999; Ansons et al., 2001; Grifn and Grisham, 2002;
refraction data (estimated by y-intercept) are similar to Taylor and Hoyt, 2005). We are carrying out new
published studies (Mohindra and Held, 1981). The studies to investigate whether style of near cue use can
photorefraction camera ash was mounted above the characterise diagnosis-specic clinical patterns. The
camera and so we were only able to refract in one gender differences we report here highlight the impor-
meridian. It is possible that our results were inuenced tance of considering gender as an additional variable.

2008 The Authors. Journal compilation 2008 The College of Optometrists


124 Ophthal. Physiol. Opt. 2008 28: No. 2

The evidence for gender differences being signicant AR600-A in an adult population with healthy eyes. Optom.
in the prevalence of ocular problems in older children is Vis. Sci. 80, 245251.
weaker, but this is not necessarily surprising because Ansons, A., Trimble, R., Davis, H. and Mein, J.(2001)
there is an extensive theoretical and experimental Diagnosis and Management of Ocular Motility Disorders.
Blackwell Science, Oxford.
literature describing processes that allow for sensory
Aslin, R., Shea, S. and Metz, H. (1990) Use of the Canon R-1
and motor adaptation and exibility of the developing
autorefractor to measure refractive errors and accommoda-
visual system in relation to, and to compensate for, tive responses in infants. Clin. Vis. Sci. 5, 6170.
environmental, anatomical and developmental variabil- Atkinson, J.(2000) The Developing Visual Brain. Oxford
ity (e.g.Ciuffreda et al., 2005; Schaeffel and Howland, Medical Publications, Oxford.
1991; Schaeffel et al., 1993; Schor, 1986a; Schor et al., Attebo, K., Mitchell, P., Cumming, R., Smith, W., Jolly, N.
1992; Schor and Horner, 1989; Ojaimi et al., 2005). and Sparkes, R. (1998) Prevalence and causes of amblyopia
Perhaps a genetically determined gender bias may be in an adult population. Ophthalmology 105, 154159.
another factor that the developing system needs to Banks, M. S. (1980) The development of visual accommoda-
overcome. The later gender differences in refractive tion during early infancy. Child Dev. 51, 646666.
error or strabismus can be confounded by environmen- Birch, E., Gwiazda, J. and Held, R. (1982) Stereoacity
development for crossed and uncrossed disparities in human
tal inuences such as close-work load, particularly in the
infants. Vis. Res. 22, 507513.
eld of refractive error (Parssinen et al., 1989; Adams
Blackie, C. and Howland, H. (1999) An extension of an
and McBrien, 1992; Zylbermann et al., 1993; Simensen accommodation and convergence model of emmetropization
and Thorud, 1994; Ehrlich et al., 1997; Flitcroft, 1998; to include the effects of illumination intensity. Ophthalmic
Blackie and Howland, 1999; Hung and Ciuffreda, 1999; Physiol. Opt. 19, 112125.
Goldschmidt, 2003), so very early differences may not Blade, P. J. and Candy, T. R. (2006) Validation of the
be responsible for much (or any) of the variance later PowerRefractor for measuring human infant refraction.
on. Possible gendernearwork interactions are less easy Optom. Vis. Sci. 83, 346353.
to explain in terms of anisometropia (Pointer and Bland, J. M. and Altman, D. G. (1986) Statistical methods for
Gilmartin, 2004; Garcia et al., 2005) and intermittent assessing agreement between two methods of clinical mea-
exotropia (Kushner, 1999), so it is still possible that very surement. Lancet 1, 307310.
Bland, J. M. and Altman, D. G. (1999) Measuring agreement
early differences in styles of near cue use could subtly
in method comparison studies. Stat. Methods Med. Res. 8,
inuence the development of later refractive error and
135160.
binocularity. Our ndings and those of others (Held Braddick, O. and Atkinson, J. (1979) Accomodation and
et al., 1980, 1984; Birch et al., 1982) suggesting that acuity in the human infant. In: Developmental Neurobiology
differences rapidly disappear, may even provide support of Vision (ed. R. Freeman), Plenum Press, New York, pp.
for the stronger role of environmental and developmen- 289300.
tal inuences over innate ones. Braddick, O., Atkinson, J., French, J. and Howland, H. (1979)
Our non-cycloplegic method of assessing refractive A photorefractive study of infant accommodation. Vis. Res.
state makes it impossible to differentiate between true 19, 13191330.
refractive error and accommodative inaccuracy, so Brookman, K. (1983) Ocular accommodation in human
many questions remain. The evidence we present here, infants. Am. J. Optom. Physiol. Opt. 60, 9199.
Chen, P. C., Chang, R. J., Lee, D. A. and Wheeler, N. C. (1996)
and our interpretation of this evidence, however, offers
Prevalence of ocular disorders among 6- and 7-year-olds in
a possible explanation for some of the later gender
Santa Monica, California. J. Am. Optom. Assoc. 67, 358365.
differences in binocular vision development. Choi, M., Weiss, S., Schaeffel, F., Seidemann, A., Howland,
H., Wilhelm, B. and Wilhelm, H. (2000) Laboratory, clinical,
Acknowledgement and kindergarten test of a new eccentric infrared photore-
fractor (PowerRefractor). Optom. Vis. Sci. 77, 537548.
This study was supported by MRC grant G9608874N. Ciuffreda, K., Roseneld, M. and Chen, H. (1997) The AC/A
ratio, age and presbyopia. Ophthalmic Physiol. Opt. 17, 307
315.
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non-signicant.
a literature review. Eye 6, 154160.

2008 The Authors. Journal compilation 2008 The College of Optometrists

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