JOURNAL
OF EXPERIMENTAL
CHILD
Development
PSYCHOLOGY
200-216 (1990)
of Looking with Head and Eyes
BRIGID M. DANIEL University
50,
AND DAVID N. LEE
of Edinburgh.
Edinburgh.
Scotland
Research into stabilization of gaze has concentrated on how the eyes counterrotate to compensate for head rotation. There is little information on how head movements function as an integral part of gaze stabilization. The head and eye coordination of six adults and six infants was tested under two conditions: tracking a moving target when the body was stationary; fixating a stationary target when the body was turning. Under each condition, both infants and adults turned their heads more than their eyes in stabilizing gaze. The infants were tested at 3-week intervals between the ages of 11 and 28 weeks. During this period, the precision with which head turning was coupled to their own or the target movement developed to near adult level, showing rapid growth between I I and 16 weeks. However, the infants’ ability to couple the eyes onto the target did not change over the tested period, remaining much less precise than the adults’. These findings have important implications for the assessment of abnormal gaze stabilization, which could facilitate the early diagnosis of perceptuomotor dysfunction. Q 1990 Academic Prew. Inc. INTRODUCTION
Catching a ball requires keeping your eye on it. Walking around requires looking where you are going to put your feet. In general, accurate control of looking is a prerequisite for accurate visual control of movement. This paper reports a study of the development of looking skill in 1 I- to 28-week-old infants. In order to pick up detailed information about a feature of the environment, the line of gaze-the imaginary line through the fovea and the center of the pupil-must be kept directed at the feature. This requires the feature be kept in the field of view by appropriate movements of the Our thanks to David Young. Jennifer Wishart, Jim Demetre. Jim Cuthbert. Jim Duncan, and Bill Robertson for help with the experiments. The research was supported by a postgraduate studentship from the Science and Engineering Research Council to B.M.D. and forms part of a Ph.D. thesis at Edinburgh University. It was also supported by research grants to D.N.L. from the Medical Research Council and the U.S. Air Force European Office of Aerospace Research and Development. Requests for reprints should be addressed to D. N. Lee, Psychology Department. University of Edinburgh. 7 George Square. Edinburgh EHS 9JZ. Scotland. 200 0022-0965190 $3.00 Copyright All right,
D 1990 by Academic Press. Inc. of reproduction in any form reserved
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head, which may necessitate twisting the body as well as turning the head. Thus, stabilizing gaze on an object when the body and/or object is moving generally requires tracking the object both with the field of view (head tracking) and with the line of gaze within the field of view (eye tracking). In animals, such as owls, with small range of eye movement, head tracking is the prime means of stabilizing gaze. Research into gaze stabilization has concentrated mainly on adult performance and has been preoccupied with reflex response. Though it has long been recognized that vestibular information alone is not sufficient for gaze stabilization (Kornhuber, 1974; Schmid, Buizza, & Zambarbieri, 1985) research has nevertheless primarily examined how the vestibular system drives “reflex” eye movements to compensate for imposed head movements (Barnes, 1980; Melvill Jones, 1976; Outerbridge & Melvill Jones, 1971). This emphasis on vestibular reflex activity neglects the fact that vision is generally essential in stabilizing gaze (Biguer & Prablanc, 1981; Owen & Lee, 1986). It also presupposes that stabilization is principally achieved by eye movements and ignores the fact that head movements are generally necessary to keep the target properly within the field of vision. Work on the early development of gaze stabilization, both when tracking moving objects and when compensating for body movement, has also been limited by concentrating upon reflex response and by artificially restricting head movements. These studies on infants have shown that vestibularly driven eye movements occur very young: within 20 to 30 days of birth > 84% of normal-birthweight human infants show appropriately directed vestibular nystagmus in response to whole body oscillation, when blindfolded to eliminate visual information (Eviatar, Eviatar, & Naray, 1974). By 3-6 months, vestibular responses have matured, a development which parallels acquisition of head and postural control (Eviatar, Miranda, Eviatar, Freeman, & Borkowski, 1979; Illingworth. 1983). Although several studies have looked at compensatory eye movements incident on head movement (Goodkin, 1980; Regal, Ashmead, & Salapatek, 1983; Roucoux, Culee, & Roucoux, 1983; Tronick & Clanton, 1971), none has investigated the pattern of compensation for externally imposed body movement with the head free to move. Much useful visual information would be lost if a baby were unable to use the visual system effectively while being carried, which for babies is a very common experience. Similarly, studies on visual control of gaze stabilization have restrained the head and concentrated on the pattern of eye movements produced when the whole visual field moves around the subject (the optokinetic response), and when a small target moves (visual pursuit). Optokinetic following can be demonstrated in newborns (McGinnis, 1930) but shows immature characteristics (Atkinson & Braddick, 1981; Held, 1985; Kre-
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menitzer, Vaughan, Kurtzberg, & Dowling, 1979). Visual tracking that has smooth periods rather than being largely saccadic only begins to emerge at 8-12 weeks of age (Aslin, 1981). With adults it has been shown that in a natural situation when the head is free to move, it is used for much of the tracking of a moving target and also allows better accuracy in pointing and aiming tasks (Bard & Fleury, 1986; Ripoll, Bard, & Paillard, 1985). In those few studies of infants which have no restricted head movement two main findings emerge: head and eye movements are quite well coordinated (Barten, Birns, & Ranch, 1971; Trevarthen. 1984) and smooth looking patterns involving head and eyes occur before smooth pursuit with the eyes alone (Aslin, 1981). The aim of the present study was to measure the development of gaze stabilization in infants, under as natural conditions as possible that allowed the head free movement, both when fixating on a moving target and when compensating for body movement. If accurate gaze stabilization is fundamental to the accurate localization of objects with respect to the trunk, it should be well developed by 18-20 weeks when infants start reaching accurately (von Hofsten, 1980). It is likely, therefore, that important developments in stabilization occur before 20 weeks of age. In the present study, the development of looking behavior was charted from 11 to 28 weeks. Considerable improvements in head control were expected to occur during the ll- to 20-week period. METHOD
Subjects
After securing ethical approval, names of possible subjects were obtained from the birth records at a local maternity hospital. Six normal and healthy infants were recruited, three girls and three boys, and all completed the study. As indicated above, much of the relevant research with adults as well as with infants has concentrated on gaze stabilization under experimental conditions of restricted head movement. Single session data were therefore also gathered from six adult subjects (mean age, 29 years; SD, 6 years, with normal or corrected-to-normal vision) to compare with the infant data. Procedure
Infants were tested every 3 weeks between the ages of about 11 and 28 weeks giving a total of six sessions per baby. When a session had to be rerun because the baby had been fussy, or because of technical problems, it was scheduled within a few days of the original session. The mother sat, with the infant on her lap, on a chair on a turntable,
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FIG. 1. An infant taking part in the experiments. Note the headband, to which are attached two Selspot lights to record head orientation, and the eog electrodes to record eye orientation.
which could be rotated to and fro or held fixed (Fig. 1). The turntable was centered within a framework which supported a vertical adjustable strut that could be moved in an arc around the chair (Fig. 2). At the end of the strut, at the baby’s eye level, was attached a small electric motor with its axis pointing toward the baby. Small toys, about 6 cm across, were attached to the motor axis and served as visual targets for the infant. To keep the child’s attention, the toy was sometimes rotated by the motor, sometimes kept still, and sometimes quickly exchanged for another one. An experimental session comprised five blocks of four 15set trials. In each block the following four conditions were presented in random order:
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!A
FIG. Selspot
2. Side lights.
and top
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apparatus,
showing
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of the
Target moving regularly. The chair was fixed and the target was moved approximately sinusoidally between positions 50” of either side of the baby’s medial plane, at about 0.2 Hz. Target moving irregularly. With the fixed chair, the target was moved irregularly within the same 100” range and with about the same peak velocity of 125Y’. Chuir moving regularly. The target was fixed straight ahead of the baby with the chair in “zero” position and the chair was then rotated approximately sinusoidally between positions 50” of either side of the center, at about 0.2 Hz. Chair moving irregularly. The same as “chair moving regularly” except that the chair was moved irregularly within the same 100” range with about the same peak velocity of 125Y’. The motions of the target and chair (which were moved by hand) were monitored together with the infant’s head and eye movements on a Selspot system. Infrared light-emitting diodes (lights) were mounted on the chair (lights E and F, Fig. 2) and were viewed by an overhead Selspot camera with its optical axis coincident with the vertical axis of rotation of the chair, which was indicated by another light attached to the top of the frame (light A). As the target was beyond the field of view of the camera, its position was given by a reference light (D) attached to a cross-hair running through the center of the frame out to the target. The coordinates of the eyes in a horizontal plane were recorded by two lights (B, C) mounted above the eyes on a soft headband worn by the subject. The coordinates also gave the angle of rotation of the head relative to
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the environment, The orientation of the eyes in the head was recorded by electrooculography (eog): three miniature eog electrodes were attached, one at each outer canthus and one on the forehead to act as earth (Fig. 1). The DC analog signal from the eog was passed through an optical isolator and a preamplifier, and digitized by the Selspot system. The light and eog data were sampled during a period of 3 ms, at a rate of 62.5 Hz and recorded on a PDPl1/34 computer. Each session was also videotaped. At the beginning of the session the skin around the eyes was washed and the miniature eog electrodes were attached. Once the headband and lights on the head were in place, the mother sat in the chair with the baby on her lap (see Fig. 1). The trials were begun when the child’s attention was fixed on the target. If the baby showed signs of distress or fussiness the session was stopped and, if possible, continued after a break. If this was not possible the mother was asked to come back within the next day or two to repeat the session. The procedure for the adults was similar except that they were tested for only one session each and the target was a small spot, rather than a toy. The subject sat on the chair and the target and chair position were adjusted so that the subject’s head was over the center of rotation of the chair and the eyes were level with the target. The subject was asked to fixate the target and to track it with whatever movements felt comfortable. while keeping the shoulders fixed relative to the chair. Basic Measures
The development of eye movements in infancy has been well documented, but the use of the head in stabilizing gaze has not received the same attention. Figure 3 shows the typical results obtained in the present experiments. It shows that much of the target tracking was in fact performed by the head. Therefore the present study focused on measuring the development of head control in stabilizing gaze. The analyses were based on the following measures: Turgetlchuir angle. This is the direction of the target with respect to the chair. Referring to Fig. 2, it is the angle between the vertical plane through the center of rotation A and the target reference light D, and the vertical saggital plane of the chair. The latter was perpendicular to the (horizontal) line EF joining the lights on the chair. Since the optical axis of the Selspot camera was vertical, the target/chair angle equaled the angle between the camera image of AD and the perpendicular to the image of EF. When the target was straight in front of the chair, the target/chair angle was zero; when the target was to the left or right the angle was negative or positive, respectively (Fig. 4). Head/chair angle. This is the direction of facing of the head with respect to the chair. Referring to Fig. 2, it is the angle between the
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Moving Target
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FIG. 3. The performance of one infant with regular movement of the target and chair. Left-hand panels, first test session, aged 11 weeks. Right-hand panels. last session, aged 28 weeks. Broken line, target/chair angle.
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He.dl.tha,r Anglp
positive FIG. 4. Showing target and (ii) moving chair
eye/head, condition.
head/chair,
and target/chair
angles
in (i) moving
(vertical) saggital plane of the chair, as defined above, and the saggital plane of the head. The latter is perpendicular to the line BC joining the lights over the eyes and is taken to be vertical. The head/chair angle was measured as the angle between the Selspot camera images of EF for the chair and BC for the head. When the head was facing straight ahead with respect to the chair the head/chair angle was zero; when it was facing to the left or right the angle was negative or positive, respectively (see Fig. 4). Performance
Measures
The above data were used for all analyses of head movement. In order to obtain a meaningful measure of the infants’ capability at each age, it was necessary to omit sections where the infant was obviously not attending to the target. The videotapes revealed that when infants were attending to the target they actively used their heads. This was clearly reflected in the Selspot records by sections where the head/chair and target/chair angle graphs were of similar form, though not necessarily equal in amplitude or precisely in phase. Lapses in attention were conversely reflected as sections where the head/chair angle either went in a different direction from the target/chair angle or remained relatively constant. Therefore, the graphs from each trial were inspected and those sections which indicated clear lack of attention were omitted from the analysis. Head/target movement ratio. This is the ratio of the standard deviations of the head/chair angle and the target/chair angle time series. It provides an average measure, on each trial, of the amount the head moved compared with the amount the target or chair moved, without reference to the relative frequency and phase of the movements. Head/target correlation. Maintaining gaze on a moving object, or on a stationary object when the body is turning, requires prospective control: the relative movement between the object and the body has to be an-
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ticipated sufficiently far in advance to enable gaze to be synchronized with the movement. This does not necessarily imply that the head movement has to be precisely coupled to the target or chair movement: the head could, in principle, be moved with the target or chair in a relatively crude way, with precise prospective control of gaze being left to the eyes. How precisely head movement is, in fact, coupled to target or chair movement was measured by the cross-correlation between the head/chair angle and the target/chair angle time series (the head/target correlation). The analysis of the six adults’ data (see below) indicated that in mature skilled performance the head is linearly coupled to the target or chair movement. Therefore the cross-correlation between the head/chair and target/chair angles was used as a measure of developing skill in the infants. Head/target peak correlation and head/target lag. More refined measures of skill can be derived by considering how the head might be coupled to the target. Perfect coupling (cross-correlation of 1.O) requires perfect visual prospective control. Assuming there is a visuomotor delay between registering and putting into action the visual information, then the information must precisely predict the relative position and motion of the target and chair at this delay time ahead and the head must be precisly controlled on the basis of this information. There are thus two possible sources of error in performance: (i) in the intrinsic information about visuomotor delay and (ii) in matching the head movement to the form of movement of the target or chair, independent of synchronizing with the movement. These two errors were measured by shifting the head/chair angle time series with respect to the target/chair angle time series and finding the time-shift which yielded the maximum cross-correlation between the series. This cross-correlation (the head/chair peak correlation) was taken as a measure of the infant’s ability to match the target or chair movement with its head. independent of synchronizing with the movement. The time-shift that yielded the maximum crosscorrelation (the head/target lag) was taken as a measure of error in intrinsic information about visuomotor delay. When the infant was not attending, the head/target peak correlation was unusually low. To avoid such spurious low values distorting the mean results, data sections yielding a head/target peak correlation less than 0.5 were eliminated. This was, in fact, necessary in very few cases. Gaze velocity error. How well the line of gaze was coupled to the target by means of eye movements operating within the moving field of view of the head was measured as follows. First, the “ideal” eye/head angle (i.e., the angle required to fixate the target) was calculated at each sample point. This was taken as the angle between the line joining the target to the midpoint (the “cyclopean eye”) between the lights (B, C) over the eyes and the line perpendicular to BC (see Fig. 4). According
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to whether the eyes pointed left, straight ahead, or right the angle was negative, zero, or positive. (It should be noted that the sum of the ideal eye/head angle and the head/chair angle is frequently referred to in the literature as the “angle of gaze,” implying that if the angle equals the target/chair angle then the eyes are directed at the target. However, this only applies if the target is an infinite distance away. In general, the socalled “angle of gaze” has no real meaning for vision: it is generally greater than the target/chair angle, its magnitude depending on the proximity of the target (see Fig. 4, also Owen & Lee, 1986)). Next, the eog was calibrated. Since infants cannot be relied upon to fixate a static calibration point, calibration was based on the experimental trials when the eyes were moving. The time series for the eog and ideal eye/head angle were inspected and sections picked out where the series showed a matching pattern. For each of these sections, the linear regression of ideal eye/head angle on eog was calculated, since eye/head angle is a linear function of eog voltage, viz. eye/head angle = wz x (eog voltage) + c.
(1)
If the correlation coefficient was greater than 0.97 (indicating that the eyes were closely tracking the target), then the regression slope and intercept were accepted as estimates of the slope m and intercept c in Eq. (1). However, when testing the infants, problems such as crying, yawning, sweating, and occasional attempts to pull the electrodes off disturbed the eog recording, changing the intercept c (the base level) and, to a lesser extent, the slope m (the gain). To avoid the problem of the drift of the intercept, it was decided to use eye/head angular velocity instead of eye/head angle. The relation between eye/head angular velocity and eog is obtained by differentiating Eq. (1) with respect to time: eye/head angular velocity
= m x (rate of change of eog voltage).
(2)
To estimate the slope m (the same as in Eq. (l)), the ideal eye/head angle and eog time series were differentiated and smoothed using a moving Gaussian profile filter spanning 36 data points (576 ms) to yield time series for ideal eye/head angular velocity and rate of change of eog. The former time series was then regressed on the latter and the slope of the linear regression was taken as the estimate of the slope m in Eq. (2). The mean slope, computed from sections of high correlation between ideal eye/head angle velocity and rate of change of eog for individual trials in a session, was used to calibrate the eog for the whole session. For all the infants the slope remained quite constant over many sessions and an average value was used for those sessions where it was not possible to obtain sufficient sections of high correlation for calibration. The root mean square difference between the actual eye/head angle
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velocity (as measured by the calibrated rate of change of eog) and the ideal eye head angle velocity time series was taken as a measure of gaze velocity error. The measure for individual trials (not including large velocity differences attributed to blinks. etc.) were averaged to produce a mean gaze velocity error for each session. RESULTS
To examine the average changes in performance over age and the effect of chair versus target movement. the values of the above five performance measures were first computed for each of the 20 trials in each session for each child. The mean and standard deviation of each performance measure across the 20 trials in a session were then taken as estimates of, respectively, the mean performance and inconsistency of performance of the child at that age on that measure. Averaging these individual estimates over the six infants yielded estimates of the average mean performance and the average inconsistency of performance on each measure at each age. Similarly, estimates were calculated for the six adult subjects, who were treated as belonging to a single age group. Effects of age and condition were tested for by a nonparametric analysis of variance (Bradley, 1968). A Page’s L test was applied to any significant trend to see if it was monotonic. Headlturget movement ratio. Figure 5a shows that both the infants and adults used the head a great deal in stabilizing gaze. On average, there was a significant monotonic increase with age of the infants in mean head/target movement ratio up to around 90% (Friedmans x?(5) = 17.95. p < 0.003, two-tailed; Page’s L = 515, p < 0.001, one-tailed). The SD of the ratio, measuring inconsistency of head use, remained constant and low. Interestingly. the mean head/target movement ratio increased rapidly up to 16 weeks, which is when visually guided reaching normally starts developing (von Hofsten, 1980, 1986). The video records, in fact, frequently showed the infants at 16 weeks and older actively orienting toward the target as if to possess it. In contrast, the adults were simply looking at the target and their head/target movement ratio was much lower on average. Whether the target or the chair moved made no significant difference to the average mean or SD of the head/target movement ratio, either for the infants or the adults (Fig. 6a). Head/target correlation. Figure 5b shows the average change over age in how well the head movement was coupled to the target/chair movement. The mean head/target correlations increased significantly and monotonically with age (x2(5) = 22.10, p < 0.0005; L = 528, p < 0.001, one-tailed), indicating increasing precision in coupling. At the same time. the SD of the head/target correlations decreased significantly with age (xr’(5) = 19.45, p < 0.002; L = 518, p < 0.001, one-tailed), indicating
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5. Changes over age in the average mean and SD performance together with the average results of six adults.
measures
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increasing consistency of coupling. By 28 weeks of age, the infants were performing close to adult level on these measures. There was no significant difference in performance when the target rather than the chair was moved, as measured by either the mean or the SD of head/target correlation for infants or adults (Fig. 6b).
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Head/target peak correlation. Figure 5c shows the average change over age in how well the movement of the head matched the form of the target/chair movement, independently of synchronizing with it. There was a significant monotonic upward trend with age (xY’(~) = 16.34, p < 0.006; L = 517.5, p < 0.001. one-tailed). indicating improved matching
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of movement. In addition, the SD showed a significant monotonic downward trend (x?(S) = 13.86, p < 0.02; L = 517.5, p < 0.001, one-tailed), indicating greater consistency in performance with age. By 28 weeks of age, the infants were performing about the same as the adults’ on both of these measures. For neither the infants nor the adults was there any significant difference in these measures when the target rather than the chair was moved (Fig. 6~). Head/target lag. Figure 5d shows the average change over age in how well the head movement was synchronized with the target/chair movement. There was a significant monotonic decrease in head/target lag over age &r’(5) = 14.97, p < 0.011; L = 520.5, p < O.OOl), indicating increasing efficiency in accommodating to visuomotor delay. The average mean lag at 28 weeks was small but significantly greater than the adults’ (t = 1.861, p < 0.05). The average SD of the lag also monotonically decreased with age (x?(5) = 14.97, p < 0.011; L = 509, p < O.OOl), indicating increasing consistency in performance. When the chair rather than the target moved, the average mean lag was smaller (Fig. 6d). This was not significant for the average results but was for the individual results @ < 0.0005, binomial test). Gaze velocity error. There was no significant trend over age in mean or SD of gaze velocity error (Fig. Se). At 28 weeks of age, the mean gaze velocity errors of the infants were considerably higher (t = 9.477, p < 0.0001) than the adults’, which were consistently low. It was possible that the lack of reduction in gaze velocity error with age was due to the infants moving their eyes around the target more as they got older, thus increasing the gaze velocity error. To test this, we computed the mean gaze velocity errors for static target trials, which had been recorded on several sessions, but no significant change over age was found (Fig. 5e). It therefore appears that the infants did not improve, from 11 to 28 weeks, in their ability to track the target smoothly with their eyes. On average, neither the mean nor the SD gaze velocity error was significantly different when the chair rather than the target was moved, for either the infants or the adults (Fig. 6e). DISCUSSION
The infants all showed development in prospective control of the head from I1 to 28 weeks of age. The head/target correlation increased during this period, indicating improved ability to couple the movement of the head to the target. The two components of this ability-matching the form of the target or chair movement with the head, and synchronizing with the movement-both improved: peak head/target correlation increased with age and head/target lag decreased. During this period, the head was generally moved vigorously.
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The inferior accuracy in eye tracking of the infants relative to the adults, as measured by gaze velocity error, could be due to their being less efficient in the use of information for controlling smooth eye movements. The examples in Fig. 3, taken from the first and last sessions of one infant, show that especially when the target was moving eye movements were quite saccadic. In spite of this, the infants were able to pick up sufficient visual information for effective head tracking. The infants turned their heads through a greater angle in tracking the target as they got older (increasing head/target movement ratio). This increase makes sense since it mirrors the infants’ increasing accuracy in coupling head movement to the target. But why did the infants show a significantly higher head/target movement ratio than the adults, who had slightly more accurate head movements? Two possibilities are: Immaturity in structure and control of infant eyes. At one week of age the peripheral retina is structurally mature, but the fovea is very immature and develops over several months (Abramov, Gordon, Hendrickson, Hailine, Dobson, & La Bossiere, 1982). There is evidence, based on performance, for a more sensitive central region by 2 months, but, whereas peripheral acuity plateaus at 4 to 5 months, fovea1 acuity continues to develop over the first year of life (Sireteanu, Kellerer, & Boergen, 1984). It has been suggested that infants’ greater use of the head in tracking is due to this fovea1 immaturity, since their gaze-stabilization behavior is similar to that of afoveate animals (Roucoux et al., 1983). It has also been observed that children with a severe visual deficit follow a moving target mainly by turning their heads (Jan et al., 1986). Even by the end of the present longitudinal study, the infant eye movements were saccadic. This suggests that control of smooth eye movements was still developing. If head control were more developed than eye control, then performing the bulk of tracking with the head would be a good strategy. Different nature oj‘the task for the infant. In infants there is a strong compulsion to explore both visually and manually and it was apparent during testing that a prime motivation in tracking was to grab the target. The fact that the amount of head movement increased up to around the time that visually guided reaching starts developing supports the notion that the infants were attempting to keep aligned on the target in order to perform an act upon it, not simply to watch it. In adults stabilizing the head with respect to the target improves performance in actions such as basketball shooting (Ripoll et al., 1985) and reaching (Biguer, Prablanc, & Jeannerod, 1984). In summary, 20-week-old infants show prospective control at near adult level in coupling head movement to a visual target, whether it is the target or infant which is moving. In contrast, the ability to couple eye movement to the target within the moving visual field of the head
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is relatively immature at 28 weeks. There is likely to be a strong relationship between the development of prospective control of gaze and performance in visually guided acts such as reaching. This deserves investigation. It is also important to examine the interaction between the extent of head movement and the task being performed: accuracy of visually guided movements in infants may be related to the ability to accurately align the head with the target. As gaze stabilization is fundamental to visually controlling action, its disruption could have widereaching effects. Greater understanding of normal and abnormal development of head and eye coordination could, therefore, have important diagnostic and therapeutic consequences. REFERENCES Abramov, I., Gordon, J.. Hendrickson, A., Hailine, Dobson. V.. & La Bossiere. E. (1982). The retina of the human infant. Science, 217, 265-267. Aslin, R. N. (1981). Development of smooth pursuit in human infants. In D. F. Fisher, R. A. Monty. & J. W. Senders (Eds.). Eye mo\‘ements: Cognition and visual percepfion. Hillsdale, NJ: Erlbaum. Atkinson, J.. & Braddick, 0. (1981). Development of optokinetic nystagmus in infants: An indicator of cortical binocularity? In D. F. Fisher, R. A. Monty. & J. W. Senders (Eds.), Eye movements: Cognition and visaal perception. Hillsdale. NJ: Erlbaum. Bard, C., & Fleury. M. (1986). Contribution of head movement to the accuracy of directional aiming in a coincidence-timing task. In M. G. Wade, & H. T. A. Whiting (Eds.). Motor development: Aspects ofcoordination and control. Dordrecht: Martinus Nijhoff. Barnes, G. R. (1980). Vestibular control of oculomotor and postural mechanisms. CLinical Physics & Physiological Measurement, 1, 3-40. Barten. S.. Birns, B.. & Ranch. J. (1971). Individual differences in the visual pursuit behaviour of neonates. Child Development. 42, 313-319. Biguer. B., & Prablanc, C. (1981). Modulation of the vestibuloocular reflex in eye-head coordination as a function of target distance in man. In A. F. Fuchs & W. Becker (Eds.), Progress in oculomofor research. Amsterdam: North-Holland. Biguer. B., Prablanc, C.. & Jeannerod. M. (1984). The contribution of coordinated eye and head movements in hand pointing accuracy. E.rperimental Brain Research, 55, 462-469. Bradley, J. V. (1968). Distribution-free statistical tests. Engelwood Cliffs. NJ: PrenticeHall. Eviatar, L., Eviatar, A., & Naray. I. (1974). Maturation of neurovestibular responses in infants. Developmental Medicine & Child Neurology. 16, 435-446. Eviatar. L., Miranda, S., Eviatar, A., Freeman, K.. & Borkowski, M. (1979). Development of nystagmus in response to vestibular stimulation in infants. Annals of Neurology, 5, 508-514. Goodkin, F. (1980). The development of mature patterns of head-eye coordination in the human infant. Early Human Development, 4, 373-386. Held, R. (1985). Binocular vision-Behavioural and neuronal development. In J. Mehler & R. Fox (Eds.), Neonate cognition. Hillsdale, NJ: Erlbaum. Illingworth, R. S. (1983). The development of the infant and yoang child (8th ed.). Edinburgh: Churchill Livingstone. Jan, J. E.. Farrell, K., Wong, P. K.. & McCormick, A. Q. (1986). Eye and head movements of visually impaired children. Developmentul Medicine & Child Neurology. 28, 285293.
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Kornhuber. H. H. (1974). Nystagmus and related phenomena in man: An outline of otoneurology. H. H. Kornhuber (Ed.), Hun&o& ofsvnsory physiology (Vol. V1/2. pp. 193-232). Springer-Verlag, New York/Berlin. Kremenitzer, J. P.. Vaughan, H. G.. Jr.. Kurtzberg, D.. & Dowling. K. (1979). Smoothpursuit eye movements in the newborn infant. Child Devulopmenf, 50, 442-448. McGinnis. J. M. (1930). Eye movements and optic nystagmus in early infancy. Generic Psychological Monogruphs. 8, 32 I-427. Melvill Jones, Cl. (1976). The vestibular system for eye movement control. In R. A. Monty & J. W. Senders (Eds.). Eve mo~~ements und psychologicul processes. Hillsdale, NJ: Erlbaum. Outerbridge, J. S.. & Melvill Jones, G. (1971). Reflex vestibular control of head movement in man. Aerospuce Medicine, 42, 935-940. Owen, B. M.. & Lee, D. N. (1986). Establishing a frame of reference for action. In M. G. Wade & H. T. A. Whiting (Eds.), Motor Development: Aspects of’coordination crnd control. Dordrecht: Martinus Nijhoff. Regal, D. M., Ashmead. D. M., & Salapatek. P. (1983). The coordination of eye and head movements during early infancy: A selective review. Beha~ioural Brain Research, 10, 125-132. Ripoll, H.. Bard, C.. & Paillard, J. (1985). Stabilization of head and eyes on target as a factor in successful basketball shooting. Humun Movement Science, 5, 47-58. Roucoux. A.. Culee. C.. & Roucoux. M. (1983). Development of fixation and pursuit eye movements in human infants. Behavioural Brain Research. 10, 133-139. Schmid, R.. Buizza. A.. & Zambarbieri. D. (1985). Visual stabilization during head movement. In D. J. Ingle, M. Jeannerod, & D. N. Lee (Eds.). Bruin Mechanisnus und Sputicll Vision. Dordrecht: Martinus Nijhoff. Sireteanu, R., Kellerer. R., & Boergen. K. P. (1984). The development of peripheral visual acuity in human infants. Human Neurobiology. 3. 81-85. Trevarthen. C. (1984). How control of movement develops. In H. T. A. Whiting (Ed.), Humun motor uctions: Bernstein reassessed. Amsterdam: Elsevier Science-NorthHolland. Tronick, E., & Clanton. C. (1971). Infant looking patterns. Vision Reseurch, 1479-1486. von Hofsten. C. (1980). Predictive reaching for moving objects by human infants. Joltmu/ of Experimentul Child Psychology, 30, 369-382. von Hofsten. C. (1986). The emergence of manual skills. In M. G. Wade & H. T. A, Whiting (Eds.), Motor development in children: Aspects of’coordinution and control. Dordrecht: Martinus Nijhoff. RECEIVED:
August
25, 1988; REVISED: February
12. 1990.
OF EXPERIMENTAL
CHILD
Development
PSYCHOLOGY
200-216 (1990)
of Looking with Head and Eyes
BRIGID M. DANIEL University
50,
AND DAVID N. LEE
of Edinburgh.
Edinburgh.
Scotland
Research into stabilization of gaze has concentrated on how the eyes counterrotate to compensate for head rotation. There is little information on how head movements function as an integral part of gaze stabilization. The head and eye coordination of six adults and six infants was tested under two conditions: tracking a moving target when the body was stationary; fixating a stationary target when the body was turning. Under each condition, both infants and adults turned their heads more than their eyes in stabilizing gaze. The infants were tested at 3-week intervals between the ages of 11 and 28 weeks. During this period, the precision with which head turning was coupled to their own or the target movement developed to near adult level, showing rapid growth between I I and 16 weeks. However, the infants’ ability to couple the eyes onto the target did not change over the tested period, remaining much less precise than the adults’. These findings have important implications for the assessment of abnormal gaze stabilization, which could facilitate the early diagnosis of perceptuomotor dysfunction. Q 1990 Academic Prew. Inc. INTRODUCTION
Catching a ball requires keeping your eye on it. Walking around requires looking where you are going to put your feet. In general, accurate control of looking is a prerequisite for accurate visual control of movement. This paper reports a study of the development of looking skill in 1 I- to 28-week-old infants. In order to pick up detailed information about a feature of the environment, the line of gaze-the imaginary line through the fovea and the center of the pupil-must be kept directed at the feature. This requires the feature be kept in the field of view by appropriate movements of the Our thanks to David Young. Jennifer Wishart, Jim Demetre. Jim Cuthbert. Jim Duncan, and Bill Robertson for help with the experiments. The research was supported by a postgraduate studentship from the Science and Engineering Research Council to B.M.D. and forms part of a Ph.D. thesis at Edinburgh University. It was also supported by research grants to D.N.L. from the Medical Research Council and the U.S. Air Force European Office of Aerospace Research and Development. Requests for reprints should be addressed to D. N. Lee, Psychology Department. University of Edinburgh. 7 George Square. Edinburgh EHS 9JZ. Scotland. 200 0022-0965190 $3.00 Copyright All right,
D 1990 by Academic Press. Inc. of reproduction in any form reserved
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head, which may necessitate twisting the body as well as turning the head. Thus, stabilizing gaze on an object when the body and/or object is moving generally requires tracking the object both with the field of view (head tracking) and with the line of gaze within the field of view (eye tracking). In animals, such as owls, with small range of eye movement, head tracking is the prime means of stabilizing gaze. Research into gaze stabilization has concentrated mainly on adult performance and has been preoccupied with reflex response. Though it has long been recognized that vestibular information alone is not sufficient for gaze stabilization (Kornhuber, 1974; Schmid, Buizza, & Zambarbieri, 1985) research has nevertheless primarily examined how the vestibular system drives “reflex” eye movements to compensate for imposed head movements (Barnes, 1980; Melvill Jones, 1976; Outerbridge & Melvill Jones, 1971). This emphasis on vestibular reflex activity neglects the fact that vision is generally essential in stabilizing gaze (Biguer & Prablanc, 1981; Owen & Lee, 1986). It also presupposes that stabilization is principally achieved by eye movements and ignores the fact that head movements are generally necessary to keep the target properly within the field of vision. Work on the early development of gaze stabilization, both when tracking moving objects and when compensating for body movement, has also been limited by concentrating upon reflex response and by artificially restricting head movements. These studies on infants have shown that vestibularly driven eye movements occur very young: within 20 to 30 days of birth > 84% of normal-birthweight human infants show appropriately directed vestibular nystagmus in response to whole body oscillation, when blindfolded to eliminate visual information (Eviatar, Eviatar, & Naray, 1974). By 3-6 months, vestibular responses have matured, a development which parallels acquisition of head and postural control (Eviatar, Miranda, Eviatar, Freeman, & Borkowski, 1979; Illingworth. 1983). Although several studies have looked at compensatory eye movements incident on head movement (Goodkin, 1980; Regal, Ashmead, & Salapatek, 1983; Roucoux, Culee, & Roucoux, 1983; Tronick & Clanton, 1971), none has investigated the pattern of compensation for externally imposed body movement with the head free to move. Much useful visual information would be lost if a baby were unable to use the visual system effectively while being carried, which for babies is a very common experience. Similarly, studies on visual control of gaze stabilization have restrained the head and concentrated on the pattern of eye movements produced when the whole visual field moves around the subject (the optokinetic response), and when a small target moves (visual pursuit). Optokinetic following can be demonstrated in newborns (McGinnis, 1930) but shows immature characteristics (Atkinson & Braddick, 1981; Held, 1985; Kre-
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menitzer, Vaughan, Kurtzberg, & Dowling, 1979). Visual tracking that has smooth periods rather than being largely saccadic only begins to emerge at 8-12 weeks of age (Aslin, 1981). With adults it has been shown that in a natural situation when the head is free to move, it is used for much of the tracking of a moving target and also allows better accuracy in pointing and aiming tasks (Bard & Fleury, 1986; Ripoll, Bard, & Paillard, 1985). In those few studies of infants which have no restricted head movement two main findings emerge: head and eye movements are quite well coordinated (Barten, Birns, & Ranch, 1971; Trevarthen. 1984) and smooth looking patterns involving head and eyes occur before smooth pursuit with the eyes alone (Aslin, 1981). The aim of the present study was to measure the development of gaze stabilization in infants, under as natural conditions as possible that allowed the head free movement, both when fixating on a moving target and when compensating for body movement. If accurate gaze stabilization is fundamental to the accurate localization of objects with respect to the trunk, it should be well developed by 18-20 weeks when infants start reaching accurately (von Hofsten, 1980). It is likely, therefore, that important developments in stabilization occur before 20 weeks of age. In the present study, the development of looking behavior was charted from 11 to 28 weeks. Considerable improvements in head control were expected to occur during the ll- to 20-week period. METHOD
Subjects
After securing ethical approval, names of possible subjects were obtained from the birth records at a local maternity hospital. Six normal and healthy infants were recruited, three girls and three boys, and all completed the study. As indicated above, much of the relevant research with adults as well as with infants has concentrated on gaze stabilization under experimental conditions of restricted head movement. Single session data were therefore also gathered from six adult subjects (mean age, 29 years; SD, 6 years, with normal or corrected-to-normal vision) to compare with the infant data. Procedure
Infants were tested every 3 weeks between the ages of about 11 and 28 weeks giving a total of six sessions per baby. When a session had to be rerun because the baby had been fussy, or because of technical problems, it was scheduled within a few days of the original session. The mother sat, with the infant on her lap, on a chair on a turntable,
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FIG. 1. An infant taking part in the experiments. Note the headband, to which are attached two Selspot lights to record head orientation, and the eog electrodes to record eye orientation.
which could be rotated to and fro or held fixed (Fig. 1). The turntable was centered within a framework which supported a vertical adjustable strut that could be moved in an arc around the chair (Fig. 2). At the end of the strut, at the baby’s eye level, was attached a small electric motor with its axis pointing toward the baby. Small toys, about 6 cm across, were attached to the motor axis and served as visual targets for the infant. To keep the child’s attention, the toy was sometimes rotated by the motor, sometimes kept still, and sometimes quickly exchanged for another one. An experimental session comprised five blocks of four 15set trials. In each block the following four conditions were presented in random order:
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!A
FIG. Selspot
2. Side lights.
and top
views
of the experimental
apparatus,
showing
location
of the
Target moving regularly. The chair was fixed and the target was moved approximately sinusoidally between positions 50” of either side of the baby’s medial plane, at about 0.2 Hz. Target moving irregularly. With the fixed chair, the target was moved irregularly within the same 100” range and with about the same peak velocity of 125Y’. Chuir moving regularly. The target was fixed straight ahead of the baby with the chair in “zero” position and the chair was then rotated approximately sinusoidally between positions 50” of either side of the center, at about 0.2 Hz. Chair moving irregularly. The same as “chair moving regularly” except that the chair was moved irregularly within the same 100” range with about the same peak velocity of 125Y’. The motions of the target and chair (which were moved by hand) were monitored together with the infant’s head and eye movements on a Selspot system. Infrared light-emitting diodes (lights) were mounted on the chair (lights E and F, Fig. 2) and were viewed by an overhead Selspot camera with its optical axis coincident with the vertical axis of rotation of the chair, which was indicated by another light attached to the top of the frame (light A). As the target was beyond the field of view of the camera, its position was given by a reference light (D) attached to a cross-hair running through the center of the frame out to the target. The coordinates of the eyes in a horizontal plane were recorded by two lights (B, C) mounted above the eyes on a soft headband worn by the subject. The coordinates also gave the angle of rotation of the head relative to
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the environment, The orientation of the eyes in the head was recorded by electrooculography (eog): three miniature eog electrodes were attached, one at each outer canthus and one on the forehead to act as earth (Fig. 1). The DC analog signal from the eog was passed through an optical isolator and a preamplifier, and digitized by the Selspot system. The light and eog data were sampled during a period of 3 ms, at a rate of 62.5 Hz and recorded on a PDPl1/34 computer. Each session was also videotaped. At the beginning of the session the skin around the eyes was washed and the miniature eog electrodes were attached. Once the headband and lights on the head were in place, the mother sat in the chair with the baby on her lap (see Fig. 1). The trials were begun when the child’s attention was fixed on the target. If the baby showed signs of distress or fussiness the session was stopped and, if possible, continued after a break. If this was not possible the mother was asked to come back within the next day or two to repeat the session. The procedure for the adults was similar except that they were tested for only one session each and the target was a small spot, rather than a toy. The subject sat on the chair and the target and chair position were adjusted so that the subject’s head was over the center of rotation of the chair and the eyes were level with the target. The subject was asked to fixate the target and to track it with whatever movements felt comfortable. while keeping the shoulders fixed relative to the chair. Basic Measures
The development of eye movements in infancy has been well documented, but the use of the head in stabilizing gaze has not received the same attention. Figure 3 shows the typical results obtained in the present experiments. It shows that much of the target tracking was in fact performed by the head. Therefore the present study focused on measuring the development of head control in stabilizing gaze. The analyses were based on the following measures: Turgetlchuir angle. This is the direction of the target with respect to the chair. Referring to Fig. 2, it is the angle between the vertical plane through the center of rotation A and the target reference light D, and the vertical saggital plane of the chair. The latter was perpendicular to the (horizontal) line EF joining the lights on the chair. Since the optical axis of the Selspot camera was vertical, the target/chair angle equaled the angle between the camera image of AD and the perpendicular to the image of EF. When the target was straight in front of the chair, the target/chair angle was zero; when the target was to the left or right the angle was negative or positive, respectively (Fig. 4). Head/chair angle. This is the direction of facing of the head with respect to the chair. Referring to Fig. 2, it is the angle between the
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Moving Target
0
2
4
6
8
Time
in
10
12
14
I6
0
2
4
sets
6
8
Time
in
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8
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10
sets
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-5cm+-1.1.1.1.1.1-1. 0 2
0
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-*@J 4
4
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8
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in
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FIG. 3. The performance of one infant with regular movement of the target and chair. Left-hand panels, first test session, aged 11 weeks. Right-hand panels. last session, aged 28 weeks. Broken line, target/chair angle.
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He.dl.tha,r Anglp
positive FIG. 4. Showing target and (ii) moving chair
eye/head, condition.
head/chair,
and target/chair
angles
in (i) moving
(vertical) saggital plane of the chair, as defined above, and the saggital plane of the head. The latter is perpendicular to the line BC joining the lights over the eyes and is taken to be vertical. The head/chair angle was measured as the angle between the Selspot camera images of EF for the chair and BC for the head. When the head was facing straight ahead with respect to the chair the head/chair angle was zero; when it was facing to the left or right the angle was negative or positive, respectively (see Fig. 4). Performance
Measures
The above data were used for all analyses of head movement. In order to obtain a meaningful measure of the infants’ capability at each age, it was necessary to omit sections where the infant was obviously not attending to the target. The videotapes revealed that when infants were attending to the target they actively used their heads. This was clearly reflected in the Selspot records by sections where the head/chair and target/chair angle graphs were of similar form, though not necessarily equal in amplitude or precisely in phase. Lapses in attention were conversely reflected as sections where the head/chair angle either went in a different direction from the target/chair angle or remained relatively constant. Therefore, the graphs from each trial were inspected and those sections which indicated clear lack of attention were omitted from the analysis. Head/target movement ratio. This is the ratio of the standard deviations of the head/chair angle and the target/chair angle time series. It provides an average measure, on each trial, of the amount the head moved compared with the amount the target or chair moved, without reference to the relative frequency and phase of the movements. Head/target correlation. Maintaining gaze on a moving object, or on a stationary object when the body is turning, requires prospective control: the relative movement between the object and the body has to be an-
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ticipated sufficiently far in advance to enable gaze to be synchronized with the movement. This does not necessarily imply that the head movement has to be precisely coupled to the target or chair movement: the head could, in principle, be moved with the target or chair in a relatively crude way, with precise prospective control of gaze being left to the eyes. How precisely head movement is, in fact, coupled to target or chair movement was measured by the cross-correlation between the head/chair angle and the target/chair angle time series (the head/target correlation). The analysis of the six adults’ data (see below) indicated that in mature skilled performance the head is linearly coupled to the target or chair movement. Therefore the cross-correlation between the head/chair and target/chair angles was used as a measure of developing skill in the infants. Head/target peak correlation and head/target lag. More refined measures of skill can be derived by considering how the head might be coupled to the target. Perfect coupling (cross-correlation of 1.O) requires perfect visual prospective control. Assuming there is a visuomotor delay between registering and putting into action the visual information, then the information must precisely predict the relative position and motion of the target and chair at this delay time ahead and the head must be precisly controlled on the basis of this information. There are thus two possible sources of error in performance: (i) in the intrinsic information about visuomotor delay and (ii) in matching the head movement to the form of movement of the target or chair, independent of synchronizing with the movement. These two errors were measured by shifting the head/chair angle time series with respect to the target/chair angle time series and finding the time-shift which yielded the maximum cross-correlation between the series. This cross-correlation (the head/chair peak correlation) was taken as a measure of the infant’s ability to match the target or chair movement with its head. independent of synchronizing with the movement. The time-shift that yielded the maximum crosscorrelation (the head/target lag) was taken as a measure of error in intrinsic information about visuomotor delay. When the infant was not attending, the head/target peak correlation was unusually low. To avoid such spurious low values distorting the mean results, data sections yielding a head/target peak correlation less than 0.5 were eliminated. This was, in fact, necessary in very few cases. Gaze velocity error. How well the line of gaze was coupled to the target by means of eye movements operating within the moving field of view of the head was measured as follows. First, the “ideal” eye/head angle (i.e., the angle required to fixate the target) was calculated at each sample point. This was taken as the angle between the line joining the target to the midpoint (the “cyclopean eye”) between the lights (B, C) over the eyes and the line perpendicular to BC (see Fig. 4). According
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to whether the eyes pointed left, straight ahead, or right the angle was negative, zero, or positive. (It should be noted that the sum of the ideal eye/head angle and the head/chair angle is frequently referred to in the literature as the “angle of gaze,” implying that if the angle equals the target/chair angle then the eyes are directed at the target. However, this only applies if the target is an infinite distance away. In general, the socalled “angle of gaze” has no real meaning for vision: it is generally greater than the target/chair angle, its magnitude depending on the proximity of the target (see Fig. 4, also Owen & Lee, 1986)). Next, the eog was calibrated. Since infants cannot be relied upon to fixate a static calibration point, calibration was based on the experimental trials when the eyes were moving. The time series for the eog and ideal eye/head angle were inspected and sections picked out where the series showed a matching pattern. For each of these sections, the linear regression of ideal eye/head angle on eog was calculated, since eye/head angle is a linear function of eog voltage, viz. eye/head angle = wz x (eog voltage) + c.
(1)
If the correlation coefficient was greater than 0.97 (indicating that the eyes were closely tracking the target), then the regression slope and intercept were accepted as estimates of the slope m and intercept c in Eq. (1). However, when testing the infants, problems such as crying, yawning, sweating, and occasional attempts to pull the electrodes off disturbed the eog recording, changing the intercept c (the base level) and, to a lesser extent, the slope m (the gain). To avoid the problem of the drift of the intercept, it was decided to use eye/head angular velocity instead of eye/head angle. The relation between eye/head angular velocity and eog is obtained by differentiating Eq. (1) with respect to time: eye/head angular velocity
= m x (rate of change of eog voltage).
(2)
To estimate the slope m (the same as in Eq. (l)), the ideal eye/head angle and eog time series were differentiated and smoothed using a moving Gaussian profile filter spanning 36 data points (576 ms) to yield time series for ideal eye/head angular velocity and rate of change of eog. The former time series was then regressed on the latter and the slope of the linear regression was taken as the estimate of the slope m in Eq. (2). The mean slope, computed from sections of high correlation between ideal eye/head angle velocity and rate of change of eog for individual trials in a session, was used to calibrate the eog for the whole session. For all the infants the slope remained quite constant over many sessions and an average value was used for those sessions where it was not possible to obtain sufficient sections of high correlation for calibration. The root mean square difference between the actual eye/head angle
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velocity (as measured by the calibrated rate of change of eog) and the ideal eye head angle velocity time series was taken as a measure of gaze velocity error. The measure for individual trials (not including large velocity differences attributed to blinks. etc.) were averaged to produce a mean gaze velocity error for each session. RESULTS
To examine the average changes in performance over age and the effect of chair versus target movement. the values of the above five performance measures were first computed for each of the 20 trials in each session for each child. The mean and standard deviation of each performance measure across the 20 trials in a session were then taken as estimates of, respectively, the mean performance and inconsistency of performance of the child at that age on that measure. Averaging these individual estimates over the six infants yielded estimates of the average mean performance and the average inconsistency of performance on each measure at each age. Similarly, estimates were calculated for the six adult subjects, who were treated as belonging to a single age group. Effects of age and condition were tested for by a nonparametric analysis of variance (Bradley, 1968). A Page’s L test was applied to any significant trend to see if it was monotonic. Headlturget movement ratio. Figure 5a shows that both the infants and adults used the head a great deal in stabilizing gaze. On average, there was a significant monotonic increase with age of the infants in mean head/target movement ratio up to around 90% (Friedmans x?(5) = 17.95. p < 0.003, two-tailed; Page’s L = 515, p < 0.001, one-tailed). The SD of the ratio, measuring inconsistency of head use, remained constant and low. Interestingly. the mean head/target movement ratio increased rapidly up to 16 weeks, which is when visually guided reaching normally starts developing (von Hofsten, 1980, 1986). The video records, in fact, frequently showed the infants at 16 weeks and older actively orienting toward the target as if to possess it. In contrast, the adults were simply looking at the target and their head/target movement ratio was much lower on average. Whether the target or the chair moved made no significant difference to the average mean or SD of the head/target movement ratio, either for the infants or the adults (Fig. 6a). Head/target correlation. Figure 5b shows the average change over age in how well the head movement was coupled to the target/chair movement. The mean head/target correlations increased significantly and monotonically with age (x2(5) = 22.10, p < 0.0005; L = 528, p < 0.001, one-tailed), indicating increasing precision in coupling. At the same time. the SD of the head/target correlations decreased significantly with age (xr’(5) = 19.45, p < 0.002; L = 518, p < 0.001, one-tailed), indicating
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c
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e FIG.
infants,
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18 Age
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A&
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(Weeks)
5. Changes over age in the average mean and SD performance together with the average results of six adults.
measures
of six
increasing consistency of coupling. By 28 weeks of age, the infants were performing close to adult level on these measures. There was no significant difference in performance when the target rather than the chair was moved, as measured by either the mean or the SD of head/target correlation for infants or adults (Fig. 6b).
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b
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6. Effect of target vs. chair at six ages and of six adults.
d
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(Weeks)
movement on the mean performance measures Broken line. moving target condition.
of six
Head/target peak correlation. Figure 5c shows the average change over age in how well the movement of the head matched the form of the target/chair movement, independently of synchronizing with it. There was a significant monotonic upward trend with age (xY’(~) = 16.34, p < 0.006; L = 517.5, p < 0.001. one-tailed). indicating improved matching
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of movement. In addition, the SD showed a significant monotonic downward trend (x?(S) = 13.86, p < 0.02; L = 517.5, p < 0.001, one-tailed), indicating greater consistency in performance with age. By 28 weeks of age, the infants were performing about the same as the adults’ on both of these measures. For neither the infants nor the adults was there any significant difference in these measures when the target rather than the chair was moved (Fig. 6~). Head/target lag. Figure 5d shows the average change over age in how well the head movement was synchronized with the target/chair movement. There was a significant monotonic decrease in head/target lag over age &r’(5) = 14.97, p < 0.011; L = 520.5, p < O.OOl), indicating increasing efficiency in accommodating to visuomotor delay. The average mean lag at 28 weeks was small but significantly greater than the adults’ (t = 1.861, p < 0.05). The average SD of the lag also monotonically decreased with age (x?(5) = 14.97, p < 0.011; L = 509, p < O.OOl), indicating increasing consistency in performance. When the chair rather than the target moved, the average mean lag was smaller (Fig. 6d). This was not significant for the average results but was for the individual results @ < 0.0005, binomial test). Gaze velocity error. There was no significant trend over age in mean or SD of gaze velocity error (Fig. Se). At 28 weeks of age, the mean gaze velocity errors of the infants were considerably higher (t = 9.477, p < 0.0001) than the adults’, which were consistently low. It was possible that the lack of reduction in gaze velocity error with age was due to the infants moving their eyes around the target more as they got older, thus increasing the gaze velocity error. To test this, we computed the mean gaze velocity errors for static target trials, which had been recorded on several sessions, but no significant change over age was found (Fig. 5e). It therefore appears that the infants did not improve, from 11 to 28 weeks, in their ability to track the target smoothly with their eyes. On average, neither the mean nor the SD gaze velocity error was significantly different when the chair rather than the target was moved, for either the infants or the adults (Fig. 6e). DISCUSSION
The infants all showed development in prospective control of the head from I1 to 28 weeks of age. The head/target correlation increased during this period, indicating improved ability to couple the movement of the head to the target. The two components of this ability-matching the form of the target or chair movement with the head, and synchronizing with the movement-both improved: peak head/target correlation increased with age and head/target lag decreased. During this period, the head was generally moved vigorously.
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The inferior accuracy in eye tracking of the infants relative to the adults, as measured by gaze velocity error, could be due to their being less efficient in the use of information for controlling smooth eye movements. The examples in Fig. 3, taken from the first and last sessions of one infant, show that especially when the target was moving eye movements were quite saccadic. In spite of this, the infants were able to pick up sufficient visual information for effective head tracking. The infants turned their heads through a greater angle in tracking the target as they got older (increasing head/target movement ratio). This increase makes sense since it mirrors the infants’ increasing accuracy in coupling head movement to the target. But why did the infants show a significantly higher head/target movement ratio than the adults, who had slightly more accurate head movements? Two possibilities are: Immaturity in structure and control of infant eyes. At one week of age the peripheral retina is structurally mature, but the fovea is very immature and develops over several months (Abramov, Gordon, Hendrickson, Hailine, Dobson, & La Bossiere, 1982). There is evidence, based on performance, for a more sensitive central region by 2 months, but, whereas peripheral acuity plateaus at 4 to 5 months, fovea1 acuity continues to develop over the first year of life (Sireteanu, Kellerer, & Boergen, 1984). It has been suggested that infants’ greater use of the head in tracking is due to this fovea1 immaturity, since their gaze-stabilization behavior is similar to that of afoveate animals (Roucoux et al., 1983). It has also been observed that children with a severe visual deficit follow a moving target mainly by turning their heads (Jan et al., 1986). Even by the end of the present longitudinal study, the infant eye movements were saccadic. This suggests that control of smooth eye movements was still developing. If head control were more developed than eye control, then performing the bulk of tracking with the head would be a good strategy. Different nature oj‘the task for the infant. In infants there is a strong compulsion to explore both visually and manually and it was apparent during testing that a prime motivation in tracking was to grab the target. The fact that the amount of head movement increased up to around the time that visually guided reaching starts developing supports the notion that the infants were attempting to keep aligned on the target in order to perform an act upon it, not simply to watch it. In adults stabilizing the head with respect to the target improves performance in actions such as basketball shooting (Ripoll et al., 1985) and reaching (Biguer, Prablanc, & Jeannerod, 1984). In summary, 20-week-old infants show prospective control at near adult level in coupling head movement to a visual target, whether it is the target or infant which is moving. In contrast, the ability to couple eye movement to the target within the moving visual field of the head
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is relatively immature at 28 weeks. There is likely to be a strong relationship between the development of prospective control of gaze and performance in visually guided acts such as reaching. This deserves investigation. It is also important to examine the interaction between the extent of head movement and the task being performed: accuracy of visually guided movements in infants may be related to the ability to accurately align the head with the target. As gaze stabilization is fundamental to visually controlling action, its disruption could have widereaching effects. Greater understanding of normal and abnormal development of head and eye coordination could, therefore, have important diagnostic and therapeutic consequences. REFERENCES Abramov, I., Gordon, J.. Hendrickson, A., Hailine, Dobson. V.. & La Bossiere. E. (1982). The retina of the human infant. Science, 217, 265-267. Aslin, R. N. (1981). Development of smooth pursuit in human infants. In D. F. Fisher, R. A. Monty. & J. W. Senders (Eds.). Eye mo\‘ements: Cognition and visual percepfion. Hillsdale, NJ: Erlbaum. Atkinson, J.. & Braddick, 0. (1981). Development of optokinetic nystagmus in infants: An indicator of cortical binocularity? In D. F. Fisher, R. A. Monty. & J. W. Senders (Eds.), Eye movements: Cognition and visaal perception. Hillsdale. NJ: Erlbaum. Bard, C., & Fleury. M. (1986). Contribution of head movement to the accuracy of directional aiming in a coincidence-timing task. In M. G. Wade, & H. T. A. Whiting (Eds.). Motor development: Aspects ofcoordination and control. Dordrecht: Martinus Nijhoff. Barnes, G. R. (1980). Vestibular control of oculomotor and postural mechanisms. CLinical Physics & Physiological Measurement, 1, 3-40. Barten. S.. Birns, B.. & Ranch. J. (1971). Individual differences in the visual pursuit behaviour of neonates. Child Development. 42, 313-319. Biguer. B., & Prablanc, C. (1981). Modulation of the vestibuloocular reflex in eye-head coordination as a function of target distance in man. In A. F. Fuchs & W. Becker (Eds.), Progress in oculomofor research. Amsterdam: North-Holland. Biguer. B., Prablanc, C.. & Jeannerod. M. (1984). The contribution of coordinated eye and head movements in hand pointing accuracy. E.rperimental Brain Research, 55, 462-469. Bradley, J. V. (1968). Distribution-free statistical tests. Engelwood Cliffs. NJ: PrenticeHall. Eviatar, L., Eviatar, A., & Naray. I. (1974). Maturation of neurovestibular responses in infants. Developmental Medicine & Child Neurology. 16, 435-446. Eviatar. L., Miranda, S., Eviatar, A., Freeman, K.. & Borkowski, M. (1979). Development of nystagmus in response to vestibular stimulation in infants. Annals of Neurology, 5, 508-514. Goodkin, F. (1980). The development of mature patterns of head-eye coordination in the human infant. Early Human Development, 4, 373-386. Held, R. (1985). Binocular vision-Behavioural and neuronal development. In J. Mehler & R. Fox (Eds.), Neonate cognition. Hillsdale, NJ: Erlbaum. Illingworth, R. S. (1983). The development of the infant and yoang child (8th ed.). Edinburgh: Churchill Livingstone. Jan, J. E.. Farrell, K., Wong, P. K.. & McCormick, A. Q. (1986). Eye and head movements of visually impaired children. Developmentul Medicine & Child Neurology. 28, 285293.
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Kornhuber. H. H. (1974). Nystagmus and related phenomena in man: An outline of otoneurology. H. H. Kornhuber (Ed.), Hun&o& ofsvnsory physiology (Vol. V1/2. pp. 193-232). Springer-Verlag, New York/Berlin. Kremenitzer, J. P.. Vaughan, H. G.. Jr.. Kurtzberg, D.. & Dowling. K. (1979). Smoothpursuit eye movements in the newborn infant. Child Devulopmenf, 50, 442-448. McGinnis. J. M. (1930). Eye movements and optic nystagmus in early infancy. Generic Psychological Monogruphs. 8, 32 I-427. Melvill Jones, Cl. (1976). The vestibular system for eye movement control. In R. A. Monty & J. W. Senders (Eds.). Eve mo~~ements und psychologicul processes. Hillsdale, NJ: Erlbaum. Outerbridge, J. S.. & Melvill Jones, G. (1971). Reflex vestibular control of head movement in man. Aerospuce Medicine, 42, 935-940. Owen, B. M.. & Lee, D. N. (1986). Establishing a frame of reference for action. In M. G. Wade & H. T. A. Whiting (Eds.), Motor Development: Aspects of’coordination crnd control. Dordrecht: Martinus Nijhoff. Regal, D. M., Ashmead. D. M., & Salapatek. P. (1983). The coordination of eye and head movements during early infancy: A selective review. Beha~ioural Brain Research, 10, 125-132. Ripoll, H.. Bard, C.. & Paillard, J. (1985). Stabilization of head and eyes on target as a factor in successful basketball shooting. Humun Movement Science, 5, 47-58. Roucoux. A.. Culee. C.. & Roucoux. M. (1983). Development of fixation and pursuit eye movements in human infants. Behavioural Brain Research. 10, 133-139. Schmid, R.. Buizza. A.. & Zambarbieri. D. (1985). Visual stabilization during head movement. In D. J. Ingle, M. Jeannerod, & D. N. Lee (Eds.). Bruin Mechanisnus und Sputicll Vision. Dordrecht: Martinus Nijhoff. Sireteanu, R., Kellerer. R., & Boergen. K. P. (1984). The development of peripheral visual acuity in human infants. Human Neurobiology. 3. 81-85. Trevarthen. C. (1984). How control of movement develops. In H. T. A. Whiting (Ed.), Humun motor uctions: Bernstein reassessed. Amsterdam: Elsevier Science-NorthHolland. Tronick, E., & Clanton. C. (1971). Infant looking patterns. Vision Reseurch, 1479-1486. von Hofsten. C. (1980). Predictive reaching for moving objects by human infants. Joltmu/ of Experimentul Child Psychology, 30, 369-382. von Hofsten. C. (1986). The emergence of manual skills. In M. G. Wade & H. T. A, Whiting (Eds.), Motor development in children: Aspects of’coordinution and control. Dordrecht: Martinus Nijhoff. RECEIVED:
August
25, 1988; REVISED: February
12. 1990.
