Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665 DOI 10.1007/s00417-007-0585-6

CLINICAL INVESTIGATION

Visual fixation development in children

Eva Aring & Marita Andersson Grönlund & Ann Hellström & Jan Ygge

Received: 12 December 2006 /Revised: 2 March 2007 /Accepted: 31 March 2007 / Published online: 24 April 2007 # Springer-Verlag 2007

Abstract there were no significant differences with regard to gender Background The ability to keep steady fixation on a target or laterality in any of the investigated variables. No is one of several aspects of good visual function. However, nystagmus was observed. there are few reports on visual fixation during childhood in Conclusion This study establishes values for visual fixation healthy children. behaviour in a non-clinical population aged 4–15 years, Methods An infrared eye-tracking device (Orbit) was used which can be used for identifying children with fixation to analyse binocular fixation behaviour in 135 non-clinical abnormalities. participants aged 4–15 years. The children wore goggles and their heads were restrained using a chin and forehead Keywords Blinks . Drifts . Intruding saccades . rest, while binocularly fixating a stationary target for 20 s. Centre of gravity Results The density of fixations around the centre of gravity increased with increasing age (p<0.01), and the time of fixation without intruding movements increased Introduction with increasing age (p=0.02), while intruding saccades decreased with increasing age (p<0.01). The number of The ability to visually fixate a target is one of several blinks and drifts did not differ between 4 and 15 years, and aspects of good visual function [1]. The ability to steadily fixate is not yet developed at birth, but is usually acquired E. Aring : M. A. Grönlund : A. Hellström during the first 6 months of life [2], parallelling the Institute of Neuroscience and Physiology/Ophthalmology, maturation of the fovea and the central nervous system Sahlgrenska Academy at Göteborg University, (CNS). Since humans are equipped with foveal vision, Göteborg, Sweden where the highest visual acuity is limited to the central 1–2° A. Hellström of the visual field, the eye must be kept within this area. International Paediatric Growth Research Centre, Furthermore, any eye movement with a velocity of >5°/s Department of Paediatrics, will degrade foveal vision during fixation [3]. It is well Sahlgrenska Academy at Göteborg University, known that children with CNS lesions, and or CNS Göteborg, Sweden haemorrhage [4, 5] or neurodevelopmental disorders may J. Ygge have defective ocular motor control [6, 7], which could Section of Ophthalmology and Vision, manifest as unstable fixation. A high frequency of intruding Department of Clinical Neuroscience, Karolinska Institutet, saccades during fixation has also been described in adult Stockholm, Sweden patients with different neurological disorders, such as E. Aring (*) progressive supranuclear palsy, Friedreich’s ataxia and Department of Paediatric Ophthalmology, focal cerebral lesions [8, 9]. Monocular visual loss may ’ Queen Silvia Children s Hospital, result in fixation being disrupted by low frequency and low Sahlgrenska University Hospital/Östra, SE 416 85 Göteborg, Sweden amplitude drifts, and bilateral visual loss can present with e-mail: [email protected] nystagmus [10]. Patients with morphological changes in the 1660 Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665 macula may have stable fixation despite reduced visual 35); and IV, 13–15 years (n=30). A detailed description of acuity (20/100); thus, eyes with functional impairment the population and the ophthalmologic data [27], as well as mostly show unstable fixation (deviation of >3°), even in the orthoptic evaluation [28] has been presented elsewhere. patients with only slightly reduced visual acuity (20/25) Informed consent to participate was obtained according [11]. Some ocular and visual defects, for example congen- to the Declaration of Helsinki from all children and their ital cataract, strabismus and amblyopia, can also directly parents. The study was approved by the Ethics Committee produce unstable fixation [12], and fixation behaviour can at the Medical Faculty of the University of Göteborg, therefore be used as a marker for both CNS lesions and Sweden. ocular dysfunction. Many mechanisms are involved in keeping steady Eye movement recordings fixation on a target [13]. One such mechanism is the vestibulo-ocular reflex, which depends on the ability of the The right and left eye positions (simultaneous horizontal labyrinthine mechanoreceptors to sense head acceleration and vertical) were recorded with an infrared (IR) system [14]. Other mechanisms are the visually mediated reflexes (Orbit; (IOTA, Timrå, Sweden) [29, 30]. This IR device (optokinetic and smooth pursuit tracking), which depend on works with pulsed infrared light, which is emitted from the the ability of the brain to determine the target velocity on inside of goggles and then reflected against the ocular the retina [15] and match it with eye velocity. The surface and detected by eight detectors also situated within attentiveness and reflexes required to turn the fovea towards the goggles. The eye position signals are conducted via a the object of significance, and the ability to suppress sound card to a computer, where they are recorded. The inadequate saccades, also affect the ability to fixate [16– maximum temporal resolution of our system is 100 Hz; 18]. Furthermore, the fusional vergence in response to a the spatial resolution under optimal conditions is 0.01° and retinal disparity and the accommodative vergence affects the linearity 10% (manufacturer’s data). the fixation when there is a loss of focus [2]. Previously, During recording, the child sat comfortably in a chair. fixation stability has been studied during reading [19–21], The head was restrained using a chin and a forehead rest at when studying intruding saccades and nystagmus [8, 22, 53 cm from a computer screen, and the goggles were 23], and in studies using magnetic resonance imaging secured with a strap around the back of the head. The (MRI) [24] and position emission tomography (PET) [25]. child’s head was adjusted so that the eyes were level with The purpose of this study was to characterise fixation the centre of the computer screen. No eyeglasses were used behaviour in a non-clinical population aged 4–15 years in during the recordings, as they interfered with the function order to obtain reference values to be used in children with of the recorder, and in all cases the uncorrected visual fixation abnormalities. A preliminary report on the present acuity was adequate for seeing the stimulus. Ambient study has already been published [26]. illumination was mesopic. Before the IR recordings were performed a pre-test paradigm of two vertical and two horizontal 10° saccades Materials and methods was run. This was done since it is known that the placement of the IR goggles is important for adequate recordings and Participants to avoid crosstalk between the horizontal and vertical channels. Considerable crosstalk in the recordings from One hundred and thirty-five non-clinical participants were the pre-test paradigm led to readjustment of the goggles and studied as part of an ophthalmologic and orthoptic this procedure was repeated until a satisfactory result was evaluation (n=143) in the Department of Paediatric obtained. After the goggles were in a satisfactory position Ophthalmology at the Queen Silvia Children’s Hospital, the position of the goggles was not changed. After the Göteborg, Sweden [27, 28]. Inclusion criteria were age calibration paradigm, a stable fixation stimulus (a yellow between 4 and 15 years, birth in Sweden, and being dot subtending a visual angle of 0.3°) was shown centrally resident in Västra Götaland Region, Sweden. The children on the otherwise black computer screen for 20 s, and the (72 boys and 63 girls) were recruited from different schools child was requested and encouraged to fixate the stimulus and pre-schools within the area of Göteborg. They were and keep the eyes as steady as possible. born between 1986 and 1997 and had a mean age of 9.8 years at the time of evaluation. The aim was to recruit at Analysis least five girls and five boys from each year of age. Thus, we continued to enrol children until that number had been Eight children were rejected from the study because of reached. The children were divided into four age groups: I, 4– insufficient participation (n=3) or technical problems with 6years(n=31); II, 7–9years(n=39); III, 10–12 years (n= the recording procedure (n=5); thus, recordings from 135 Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665 1661 children were included in the analysis. About 7% of the Table 1 Showing the distance of fixations around the centre of total data points were deleted due to insufficient quality, or gravity (mean and SD) “bad recordings”. These 7% were the same in the different Age group Mean distance Mean distance year groups and included large drifts of >10° and crosstalking. Degrees SD An off-line data calibration of all four channels (right – and left eye, horizontal and vertical) of the recordings was 4 6 6.8 5.6 7–9 4.9 3.9 performed using the JR program [29], and the calibrated 10–12 3.0 3.1 data were then transferred into a computer program (Origin 13–15 2.2 2.8 7.0; Microcal, Northampton, MA, USA) for further analysis and plotting. During the total 20 s of fixation time, note was taken of the longest fixation time without interruption of Fixation time saccades (defined as rapid change of eye position in any channel of more than 3° amplitude) or drifts (defined as a Analysis of the entire 20 s of fixation recordings showed slow change in eye position in any channel of more than that the mean of the longest fixation time without 3°). Blinks were defined as large rapid changes in eye interruption by blinks, intruding saccades, or drifts in- position back and forth in all channels without an creased with increasing age. The means were 3.7, 5.0, 6.0 intersaccadic interval. This is the normal characteristic of and 6.2 s in the different age groups respectively (Fig. 1). blinks with the present recording system. The 10 best seconds with regard to fixation behaviour Blinks, drifts and saccades during the best 10 s (judged visually from the plots) were further analysed; blinks were counted, as were all types of intruding saccades The mean blink frequency of the total sample was 1.5 with amplitude >3°. Large drifts (>10°), which could blinks (range 0–9) during the best 10 s. The mean numbers correspond to head movements, were counted and removed of blinks were 1.4, 1.1, 1.6 and 2.0 in the four different age from the traces, so as not to interfere with further analysis. groups (Fig. 3). During each registration of the eye position the location The occurrence of drifts did not differ among the four was saved in the computer (in X and Y coordinates from age groups and the means were 0.1, 0.3, 0.1 and 0.1 the fixation object location). The centre of gravity (CG) was respectively (Fig. 4). However, the number of intruding calculated for each individual fixation data point and the saccades during fixation decreased with increasing age (p< distance (in degrees) with regard to the CG were assessed 0.01), and the corresponding numbers for the different age [31]. groups were 4.2, 2.8, 2.2 and 1.3 (Fig. 2).

Statistical analysis

Means and standard deviations (SD) were calculated for 20 descriptive purposes. The Spearman correlation test was r=0.2 19 95% used for continuous or non-ordered dichotomous variables, 18 p=0.02 17 and the Mann-Whitney U test for the dichotomous 16 15 variables. 14 95% 13 12 11 95% SD 10 SD 9 Results 8 seconds SD 7 95% 6 SD 50 5 50% We found that fixation behaviour and stability were age 50% 4 dependent. The density of fixations around the centre of 3 50% 2 -SD -S gravity increased (p<0.01; Table 1) and fixation time -SD 1 5% 5% 5% -SD 5% without intruding movements increased with increasing 0 age (p=0.02; Fig. 1), while intruding saccades decreased 4 to 6 7 to 9 10 to 12 13 to 15 with increasing age (p<0.01; Fig. 2). The number of blinks Age groups (Fig. 3) and drifts (Fig. 4) did not differ between the ages of Fig. 1 Box and whisker plot showing the longest period of fixation 4 and 15 years, and there were no significant differences without interrupting saccades, drifts or blinks during the total 20-s recordings in different age groups. The boxes show ±1 SD, the with regard to gender or laterality in any of the investigated whiskers show 95% and 5% intervals, the crosses show the 99% and variables. No nystagmus was observed. 1% intervals and the squares show the mean value 1662 Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665

20 r=-0.36 2.0 p<0.01 18

16 1.5 (r=-0.09) 14 (p=0.3) 95% 12 95% 95% 1.0 95% 95% 95% 95% 10

SD 8 SD 95% SD SD 6 SD 0.5 SD number of drifts number of

SD 4 SD

number of intruding saccades intruding of number 2 50% 50% 0.0 5% 50% 5% 50% 5% 50% 5% 50

-SD 0 5% 5% 5% 50% 5% 50 -S -SD -SD -SD

4 to 6 7 to 9 10 to 12 13 to 15 4 to 6 7 to 9 10 to 12 13 to 15 Age groups Age groups Fig. 2 Box and whisker plot showing the number of intruding Fig. 4 Box and whisker plot showing the number of drifts during 10-s saccades during 10-s recordings in different age groups. The boxes recordings in different age groups. The boxes show ±1 SD, the show ±1 SD, the whiskers showing 95% and 5% intervals, the crosses whiskers show 95% and 5% intervals, the crosses show the 99% and show the 99% and 1% intervals and the squares show the mean value 1% intervals and the squares show the mean value

Distribution of the fixation points around the centre density of fixations around the centre of gravity (Table 1), of gravity for the best 10 s and fixation time increases (Fig. 1). Intruding saccades decrease with increasing age (Fig. 2), while blinks (Fig. 3) The mean distance to centre of gravity decreased with and drifts (Fig. 4) do not change with age. increasing age (r=−0.4; p<0.01; Table 1). Figure 5a shows an example of a child with an unstable Methodological considerations fixation and Fig. 5b shows a child with a stable fixation (Fig. 5a and b). Fixational eye movements can be recorded using different techniques, such as electro-oculography (EOG), scleral search coils, video-oculography (VOG), scanning laser Discussion ophthalmoscope (SLO), and infrared (IR) reflection [7, 32]. We chose an IR technique for the present study since it Our results in the present study showed that as age is a non-invasive method and it requires only limited increases between 4 and 15 years, children obtain a higher cognitive effort from the child. In general, the children accepted the technique, and since the test is easy to perform

11 the cooperation was mostly very good. A limited amount (7%) of data was excluded from further analysis due to the 10 bad quality of the recordings, such as noise. 9 It has been shown that patients aged 7–64 with 8 r=0.14 strabismic amblyopia and visual acuity of 0.3–0.8 have 7 p=0.08 95% stable central fixation irrespective of whether the fixation 6 mark is a detailed object (Landolt’s C) or a dot [32]. In the 5 95% present study, the fixation target was a static high-contrast 4 95% SD dot and the child was encouraged throughout the recordings

SD 95% number of blinks number of 3 SD to try to continuously fixate the dot as stably as possible.

2 SD 50 We therefore believe that the stimulus was adequate for a

1 50% 50% 50% fixation stability study. Fixation stability and distribution

-SD can be quantified from eye movement recordings using a 0 5% -SD 5% 5% -SD 5% -S number of different methods, such as the Bivariate Contour 4 to 6 7 to 9 10 to 12 13 to 15 Ellipse Area (BCEA) [33] or the Centre of Gravity (CG) Age groups [31]. As the present material was shown not to be normally Fig. 3 Box and whisker plot showing the number of blinks during 10-s distributed, we chose to use the CG method, since unlike recordings in different age groups. The boxes show ±1 SD, the whiskers show 95% and 5% intervals, the crosses show the 99% and the BCEA method it does not rely on the assumption that 1% intervals and the squares show the mean value the data are normally distributed. Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665 1663

a study increased from a mean of 1.0/10 s in the youngest 8 RE LE group (6.0 per minute) to 2.8/10 s in the oldest group (16.8 per minute), which is in agreement with Zametkin and co- 6 workers’ finding of an increase in blinks during infancy and adolescence and an almost adult frequency at 15 years of 4 age. The only way to distinguish saccadic intrusions and 2 saccadic oscillations from nystagmus is by eye movement recordings. The presence of macro saccadic oscillation and 0 Vertical (deg.) Vertical nystagmus in healthy children should be considered abnormal, while square wave jerks up to 5° can be seen -2 in healthy individuals at any age [37]. However, more than nine square wave jerks in a minute in a young person -4 should be considered abnormal. None of the children in the -5.0 -2.5 0.0 2.5 5.0 7.5 10.0 present study showed macro saccadic oscillations or Horizontal (deg.) nystagmus, but 75 children (55%) showed one or more b saccadic intrusions >3° and 63 children (47%) showed 2 RE LE more than one saccade/10 s (corresponding to more than 9/ minute). In the present study, the number of intruding saccades 1 with an amplitude of >3° decreased from a mean of 4.6/10 s in the youngest group to 1.3/10 s in the oldest. This is in agreement with the findings of Abadi and co-workers, who 0 investigated saccadic intrusions in adults using an infrared limbal tracker [8], and of Herishanu and co-workers, who

Vertical (deg.) Vertical used an IR technique and reported a negative correlation -1 with age [38]. On the other hand, Canice McGivern and co- workers found a positive correlation of intruding saccades with age in adults aged 21–81 years measured using an IR

-2 technique [34], and Abadi and co-workers found no age -2.5 -2.0 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0 2.5 correlation of intruding saccades between the ages of 19 Horizontal (deg.) and 78 years [8]. In the present study, a level of 9 saccades/ Fig. 5 a XY plot (horizontal and vertical eye position) of a 10-s min (corresponding to 1.5 saccades/10 s) was not reached recording of a child in the present study. Note the unstable fixation. b – XY plot (horizontal and vertical eye position) of a 10-s recording of a until 12 13 years of age (group III), with means of 20, 18, child in the present study. Note that the fixation is very stable. RE 13 and 7/min in each of the four age groups. The findings right eye, LE left eye of the present study thus seem to be in accordance with several other studies. Slip of retinal image due to ocular drift may also stimulate the brain to keep a steady gaze [39], as it is a A blink is a brain stem reflex that activates the part of the fusional function. Bidirectional mostly vertical orbicularis and the levator muscle [34]; there is an and unidirectional horizontal drifts with nystagmus have interaction between blinking and the saccadic premotor been noted in monocular visual loss [10], and an increase in system at the level of the superior colliculus [35]. It has drifts in children with strabismic amblyopia has been been speculated that blinks may be involved in sensory described [40, 41]. motor processing, and may facilitate attention and motor Very few drifts were seen in the present study; five response capability. Furthermore, an increase in spontane- children had strabismus, two had amblyopia, yet none of ous blinks during childhood may reflect the maturation and these children showed any drifts at all. Two of the integrity of dopaminergic circuits in the brain [36]. strabismic children (5 and 4 years old) had normal fixation Zametkin and co-workers demonstrated that the spontane- time for their age groups, while the three others (11, 11 and ous blink rate is two blinks per minute in early infancy, 12 years old) had a shorter fixation time compared with the with an increase during childhood up to the age of 15 [36]. mean in their age group. In normal adults, a frequency of 20 blinks per minute has In the present study, both fixation time and density of been described [3]. The number of blinks in the present fixations around the centre of gravity increased with 1664 Graefe’s Arch Clin Exp Ophthalmol (2007) 245:1659–1665 increasing age. On the other hand, Canice McGivern and References co-workers found an increase in the number of saccades (>0.2°) among normal individuals aged 21–81, using an 1. 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