On the onset of eye-head coordination in infants

Behavioural Brahz Research, 49 (1992) 85-90 9 1992 Elsevier Science Publishers B.V. All rights reserved. 0166-4328/92/$05.00

85

BBR01317

On the onset of eye-head coordination in infants Henriette Bloch and Isabelle Carchon Laboratoire de Psycho-Biologic du Ddveloppement, EPHE-CNRS URA 315, Paris (France) (Received 15 August 1991) (Revised version received 5 March 1992) (Accepted 15 April 1992)

Key words: Newborn; Visual pursuit; Ocular motility; Gaze line; Head rotation; Eye-head coupling

Head movements have been studied in newborns, during a visual pursuit and in relation with ocular movements, in order to know whether head movements help the ocular activity or impede it. The infants were tested three times during the first month of life. They were placed in a seated position, with the head held upright, but free to move. The results provided evidence that eyes and head were directionally coupled at as early as 2 weeks and that the interval between eye and head rotation decreases from the age of 2-4 weeks. This suggests that the beginnings of ocular-motor coordifiation are present from the first month of life in human infants.

INTRODUCTION

There has been some question about whether human newborns c a n perform coordinated eye-head movements, or whether such coordination appears only after a few months of life. The issue is important developmentally because of its relevance to differing theoretical accounts of the nature of perceptual-motor linkages and the ontogeny of integrated behavior. On the one hand, there are clinical observations that the head can participate in the newborn visual activity; for example, neonatal assessment scales such as the Brazelton Neonatal Assessment Scale 8 classify infant pursuit differently depending on whether the pursuit is made with or without head movements. The existing experimental research 3'14'2t'22'23 has yielded mixed resuits, possibly because the behavior has been studied with different methods and has primarily used infants beyond the newborn period. Debate on the issue of neonatal head-eye coordination remains open. There are several arguments against early coordination of head and eye during perceptual activity. According to Mitkin ~9, infant head movements are reflexive and not well controlled up to the 3rd month of life.

Correspondence: H. Bloch, Laboratoire de Psycho-Biolo~e du Dfveloppement, E P H E - C N R S URA 315, 41, rue Gay-Lussac, 75005 Paris, France.

Moreover, mechanical constraints caused by the weight of the neonate's head interfere with the functioning of exteroceptively oriented channels such as vision ~5, with sensory motor consequences. Because the eye rotates abruptly upon an uncontrolled fall of the head and thus gaze cannot be stably maintained, the neonate is unable to use the head as a reference axis for posture and perception without external means of head support. In adults, coordination of the eye and head allows stable fixation through suppression and regulation ofthe VOR. Goodkin~ 4 argued that there is no tonic suppression of the VOR before the 3rd month (see also Finocchiol2). Foveal immaturity has also been considered an impediment to eye-head coordination. This immaturity has been supposed to make the newborn capable of only showing alertness, not holding attention. This distinction between 'attention getting' and 'attention holding' was originally proposed by Cohen l~ If the goal of eye-head coordination is to ensure foveal fixation, as has been assumed in adults, the neonate's visual immaturity would make such coordinations impossible. Such a functionalist point of view has been proposed for other types of early coordinations ~. On the other hand, these facts may not limit, or prevent linked eye and head movements in newborns. Uprighting reflexive movements of the head have been observed and reported a number of times ~'~3'~s. Head rotations in the horizontal plane are also observed as a component of the orientation reaction to a perceptual

86 stimulation. When the newborn is orienting, the head can be held upright for several seconds, suggesting that control of the head, even ifweak, does exist. This observation challenges the frequently implicit hypothesis that coordination requires the constituent systems to have attained the same level of functional maturity; it is obvious in the newborn that the ocular system is more well-controlledthan the motor system controlling the head. For example, although some have reported early tracking to be purely saccadic 2, other work has reported smooth pursuit interrupted by phases of gaze ~6. Barten et al. 3 also reported that some 2- to 3-day-old infants consistently show eye-head pursuit. We have also observed coordinated sequences of head and eye movements in both preterm and fullterm infants tested at a gestational age of 40 weeks 5. Although the VOR has not been studied extensively in young infants, there are reports that VOR regulation does occur when young infants are attending 24 or as the result of visual practice 6. In this case, the VOR is characterized by rapid recentrations of the eye in the orbit, resulting in the stimulus being lost only for short segments of time. None of these data are per se sufficient for denying or expecting early eye-head coordination, and more data are clearly needed. We feel that future experiments will be enhanced by the adoption of operational criteria based on a clear hypothetical definition of 'coordination'. There are numerous discrepancies about the meaning of the term in the current literature, as has been noted by Lockman ~7 and Bloch 7. It is also possible that coordinations in infancy are being missed or underappreciated because of the focus on the characteristics of coordination in the adult, as, for example, in the role of the adult VOR in stabilizing vision. The first question to be answered is whether early in life head movements a r e s o disorganized that they interfere with perceptual activity, or whether they contribute to perceptual activity. For a reliable description Of infant eye-head coordination, we propose to consider two categories of criteria: one addresses questions of mechanisms, as indexed by measures such as the assumption of a common direction of movement of eye and head and the coupling of the time-course of such movements. A second category concerns vision as an organizer of visual space, and consists of an appreciation of the perceptual changes brought on by movement. Because the eye is presumed to contain no detector of its own position (i.e. no efferent feedback), and subjects are unaware of passive eye movements 4"2~ visual direction and the position of objects in space must be estimated from what is called the 'egocenter origin', a position defined as the midpoint between the eyes and corresponding to the midplane of the head. Appropri-

ate coding of object positions in space may depend on a coincidence between the oculomotor and the headmotor space. Even if this coordination arises from maturation and/or experience, we suppose that early participation of the head in visual activity is reflected in changes in the perception of the visual world. Of course, these two categories of criteria are complementary and both merit consideration. The research presented here involves a study of visual pursuit during the first month by fullterm newborns. It was designed to investigate whether an eye-head coupling represents the beginning of coordination, and to detect possible changes in the first weeks. It also addresses the question of the goal of the coupling, whether early coordination serves first to advance pursuit itself or control the point of fixation.

PATIENTS A N D M E T H O D S

Sttbjects Twenty fullterm neonates were tested on a pursuit task. They were selected on the basis of results of the Brazelton Neonatal Assessment Scale: all were able to pursue a mobile target 30 ~ horizontally, and were classified in categories 3 or 4. Performance on this task, part of a neurological examination, does not guarantee infant performance on other pursuit tasks. 'Six infants were excluded from the sample because they experienced a state change during a session, because of illness or because of a visual problem not previously detected in the perinatal neurological examination. The data reported were obtained from 14 infants tested in 3 sessions, at ages of 3 days, and 2 and 4 weeks. Testing took place at the same time each day, after a meal when the infant was in a quiet alert state. Procedure The subject was seated in an infant seat with the head supported but free to move. Two small bright dots were applied to the infant's scalp, one on the vertex and the other midline in the preoccipital region. The pursuit target was a small red, transparent ball 4 ~ in angular subtense. This target was moved in a horizontal trajectory at 8.7~ The target's movement always started from the center of the field in front of the subject, and moved alternatively to the left and right. Extent of the movements~was 60 ~ requiring 7.6 s for a full excursion. Within a session, each subject was shown 3 trials in each direction. The total number of trials tested at each age was thus 84. Eye and head movements were filmed by two independent video cameras (Fig. 1), the two cameras were

87

i

C

EXPERIMENTAL SETTING

I MIRROR

1

vIDEOTAPE RECORDER -F

timer

VIDEOSCREEN 2 VIDEOSCREEN 1

Fig. 1. Eye and head movements filmed by two independent video cameras.

linked to a timer which allowed synchronization of their images by recording the time on each video image. Camera 1 recorded head movements by means of an over-head mirror. Images provided by this camera are an image of the reflective head dots (in the mirror), and a frontal view of the infant's head and body. Camera 2 recorded a close-up view of the upper part of the infant's face. When the infant was fixating the target at the start of a movement trial, the eyes were centered in the images of Camera 2, allowing us to measure interpupillary distance the second beforethe stimulus began to move. The measure was made frame by frame, position and the median value served as baseline. The position of the eye as well as of the head dots were analyzed frame by frame during target movement, using an x,y pointer interfaced with a computer.

RESULTS

First we measured the extent of pursuit, whenever it occurred. We then evaluated the features of ocular ac-

tivity during this pursuit, and finally, measured the characteristics of head movements and their coordination with eye movements.

Amplitude of pursuit and its relation to age The angular amplitude of pursuit was calculated for each age group. The measure was taken from measurements of successive positions of the eyes by the second camera during movement of the target, relative to t a r get position. Pursuit was considered 'disrupted' when the eyes failed to follow the target for at least i s. Disruption of pursuit was marked more often by a movement of theeyes in a direction opposite to the target's motion than by fixation. Mean values for pursuit, with ranges and standard deviations are given in Fig. 2. As can be seen in the figure, there is good consistency of responses within each age group. Pursuit increased in amplitude over the tested age range for all of the subjects, despite the fact that there was no rank order correlation for individual subjects across the three session (Kendall W=0.41). A t-test for paired samples shows no difference between 3 and 15 days, and sig-

88 50-

40-

t'

30-

20

7,*,

lo

o

-

3

f

~5

30

Days

Ages {in dogs)

Fig. 2. Angular extent of visual pursuit with age. The extreme values of pursuit are indicated for each age on the left side of the bars. Standard deviations are indicated above. nificant difference between 15 and 30 days (t=4,29; P<0.01). Features of o'e movements Two indicators were considered to evaluate the form of the oculomotor activity observed. Number ofsaeeades. The first measure evaluated was the number of saccades occurring during pursuit. In the neonates, as has been previously reported, eye displacements were predominantly saecadic. The jumps ofgaze were easily visible by eye, and were confirmed by image analysis. Pursuit remained largely saccadic up to 4 weeks. The mean number of saccades did not differ widely with age, despite the increase in amplitude of pursuit over the tested age range. The mean number of saccades per pursuit trial was 2 for neonates and 3 for 2- and 4-week-olds. Because our experimental situation did not allow precise measures of saccadie amplitude, we cannot evaluate whether the saccades of the older infants resulted in better following of the target, although we could take into account the latencies of the first and following saccades. Latency of first saccade. In neonates; the latency of the first saccade was highly variable, both within and across individuals, so a mean is not a particularly representative measure of central tendency. At 2 and 4 weeks, latency of the first saccade was less variable from trial to trial and subject to subject. The second saccade occurred with a shorter latency than the first for more than 80~o ofthe subjects. Because some subjects moved their eyes before the target began to move, the relation between the latency of the first saccade and the target position has to be considered as an approximation. There was a slight asymmetry in latency as a function of target direction; the mean latency was slightly longer for a movement to the right than to the left. Such a delay indicates that a portion of smooth

pursuit can be performed by the 2- and 4-week-olds, and suggests a relation between this initial saccade and the orthostatic (i.e. straight upright) position of the head. Latency of subsequent saccades. In neonates, there was no systematic relation found between the latencies for first and the second saccades; the second saccade occurred between 1.8 and 3 s, after target motion began, either immediately following the first saccade or after a delay. However, the eyes were not on the target along the interval between the first and second saccades. In 2- and 4-week-old infants, there was a stronger relation between the latency of the first and second saccade. The second saccade occurred at a mean of 2.8 s for 2-week-olds and 2.6 s for the 4-week-olds. Gaze was directed to the target during the inter-saccadic interval. Characteristics of head movements Four criteria were examined to assess the participation of the head in visual activity; the frequency of head movements regardless of their form or direction and the form, direction, and latency of head movements. Frequency of head movenlents. In neonates, only 28 ~o of trials did not contain a head movement, being composed only of ocular pursuit. Head movements occurred after the first or second saccade. At 2 and 4 weeks, all pursuits of the target involved a head movement component. Form of head movements. In neonates, head movements were either a rotation (76~), a lateral tilt ( 4 ~ ) or a rapid fall backward or forward (0 ~o). Rotation was defined as the head turning into the horizontal plane, with no change with respect to the line of the shoulders. A lateral tilt was defined as a movement into the vertical plane, involving a change of head position with respect to the shoulders. A 'fall' was not a literal fall, TABLE 1

Forms of head movenzents n indicates the total n u m b e r o f head m o v e m e n t s in 3-day-olds, s o m e m o v e m e n t s (5.8%) a p p e a r c o m p o s i t e a n d 'undertermined'.

Ages (days)

M VT Fall

Tihing

Rotation M

Day 3 (n = 76) Day 14-15

op

10~o

4~

50%

80.2~

30.2~

3%

0%

70~

97~

27~

0~o

0%

88~

100~

12~

(n = 125)

Day 30 0~=212)

89 because the infant's body was well supported. Falls were quite distinctive: they were not in the same direction, they were very rapid, and they disrupted pursuit. Falls were even less frequent in 2-week-olds (3 ~ ) , and were not observed at all at 4 weeks. Direction of head movements. Head rotations and lateral tilts could have been in the direction of target and eyes movements, or in the opposite direction. In 3-dayolds, tilts were always opposite to the direction of target movement, but they did not impede the pursuit. In contrast, head rotations were most often in the direction of target movement. Head rotations opposite to target and eye movements were sometimes observed at the end of pursuit, after the second following saccade, and seemed to be the cause of the cessation of pursuit. Between 2 and 4 weeks, there was an increase in the number of head rotations in the direction of target and eye movement, indicating that eyes and head are increasingly involved in a single common act. Latency of head movemems. The first head movement was always performed after a delay, after the target began to move. Even in 3-day-olds, we never observed a head movement appearing coincident with the start of target movement before an eye movement occurred.

Coupling of eye and head The interval between the first saccade and the first head movement was considered as a measure of coupling. As shown in Table II, this interval was highly variable in newborns, but decreased from 2 to 4 weeks, indicating improvement in the coordination of head and eye movements. If we consider that coordination implies a strong and constant coupling relationship between two systems, the data do not support the existT A B L E II

Latencies o f the first eye and head movements T h e latency o f the first ocular s a c c a d e is c o m p u t e d from the target starting. T h e n u m b e r s in parentheses indicate the excentricity o f the target. T h e latency o f the first head rotation is c o m p u t e d from the ocular saccade.

Ages

14 days

Latencies First ocular saccade

First head rotation

R = 1.45 s

R = 0.47 s

(12.5~) 30 days

L = 1.28 s (10.4 ~) R = 1.46 s

L = 0.51 s R = 0.34 s

02.7 ~ L = 1.31 s

(11.4 o)

L = 0.40 s

ence of such a coupling in neonates. At the same time, because the head tends to move in the same direction as the eyes even in neonates, albeit with an uncorrelated latency, we do have evidence of a beginning of such a coordination even at birth. It appeared that head rotation is controlled by the occurrence of saccades in 2- and 4-week-olds; at these ages, the rhythm of saccades was closely regulated and head movements were less variable in form and direction, evidence of the emergence of coupling. In the neonates, by contrast, the variability in both the intersaccadic intervals and latencies of head movements limited eye-head coupling.

DISCUSSION

Although visual pursuit changes character during the first month, during this interval smooth pursuit was rarely seen. Rather, the pursuits seen were discontinuous and saccadic. Nevertheless, participation of head movements in visual pursuit was seen even at birth, although not all head movements assisted pursuit at this age. Hogcever, at as early as 2 weeks, head rotations were correlated with following eye movements and are in the same direction as target movement. It may be that the limitation in eye-head coupling at birth is not only from immaturities in the system controlling head movements; there were also immaturities at this age in oculomotor functioning, specifically in the variable rhythm of the saccades seen, and in pauses in pursuit. By 2 weeks, head rotations clearly contributed to increased pursuit. Regal et al. 2~ reported that in 2-month-olds, a head movement sometimes preceded an eye movement in target tracking. This was not observed here, rather, in our infants, pursuit was initiated either by a saccade or a smooth eye displacement, which had the effect of holding gaze on the target. It is possible that our result occurred because target movement always started from the center of the field, which may be a favorable position to build a relationship between eye and head movements. This issue needs to be examined by using different target trajectories, and by looking at the development of pursuit with the head fixed. Our data suggest that eye-head coordinations do not depend on a transformation in form of pursuit, for example, from saccadic to smooth pursuit. According to Mitkin 19 a transition from purely ocular to coordinated eye-head pursuit should consist of both a reduction in saccadic amplitude and intersaceadic intervals, which he believed occurred in the second month of life. We believe that we have found an earlier transition, con-

90 sisting of an initial extended pause of gaze as shown by the latency of the first saccade. However, without having information about the orbital position of the eye in relation to target position, we cannot be sure whether the first function of head participation in visual pursuit is to allow target fixation, although it does appear that head movements first contribute to extend pursuit in young infants. To study the matter further requires studying precisely the relation between the extent of the pursuit and the form and rhythm of following eye movements. However, the first stage in building eye-head coordination may be determined by the correspondence between the upright position of the head and starting point of the target.

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