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Infants' fast saccades in the gap paradigm and development of visual attention
INFANT BEHAVIOR AND DEVELOPMENT 20 (4), 1997, Copyright 0 1997 ABLEX Publishing Corporotion
pp. 449-455
ISSN 0163-6383 All rights of reproduction in any form resewed.
Infants’ Fast Saccades in the Gap Paradigm and Development of Visual Attention MASAKO
MATSUZAWA
Shirayuri College
SHINSUKE
SHIMOJO
University of Tokyo The
saccadic reaction times (SRTs) in the overlap, no-overlap, and gap conditions of 2.5- to 12-month-old infants and adults were measured. In the overlap condition, the SRTs of younger infants were over 600 ms longer than those of older infants, whereas the SRTs in the gap condition of the younger infants were 300-350 ms, much faster than reported hitherto, and were shortened only by about 100 ms. The results indicate that the oculo-motor system and attention process for disengagement in the gap condition mature earlier than the attention process for disengagement in the overlap condition.
saccades
eye movements
reaction
times
Infants of a few months of age have difficulty orienting towards peripheral stimuli. Studies in which saccadic reaction times (SRTs) were measured demonstrated that the SRTs were longer in “overlap” than “no-overlap” condition and this tendency was more pronounced in the younger infants (Aslin & Salapatek, 1975; Johnson, Posner, & Rothbart, 1991). In the overlap condition, a fixation point remained after presentation of a peripheral target, whereas in the no-overlap condition, a fixation point disappeared upon presentation of a peripheral target. Therefore, the results (i.e., the difference between the SRTs in the overlap and no-overlap conditions of young infants), suggest that a critical factor responsible for the orientation difficulty of young infants is the inability to disengage their attention from a currently fixated stimulus (Johnson, 1990; Johnson et al., 1991). This suggestion is supported by the studies of Atkinson, Hood, Braddick, and Wattam-Bell (1988) and Atkinson, Hood, WattamBell, and Braddick (1992), who found the same pattern of results and eliminated the possibility that the effect was confounded with developmental changes in visual sensitivity by adjusting the luminance thresholds for the different age groups. More recently, Hood and Atkinson (1993) measured SRTs in “gap” condition as well as the Direct all correspondence to Masako Matsuzawa, Department of Developmental Psychology, Shirayuri College, 1-25 Midorigaoka, Chofu-shi, Tokyo 182, Japan.
aaa effect
visual attention
infants
overlap and no-overlap conditions. In the gap condition, a fixation point disappeared before the delayed presentation of a peripheral target. The SRTs in the gap condition of both younger and older infants were shorter than those in the no-overlap condition. The gap effect has been explained in two ways in studies using adults or animals-by an attentional account or an oculomotor one. The former assumes that the gap effect occurs because the attention on a fixation point is disengaged automatically by the disappearance of the fixation point in the gap condition. The disengagement of attention occurs prior to target presentation, thus makes the SRTs shorter (Fischer, 1986; Fischer & Breitmeyer, 1987; Fischer & Weber, 1993). This attentional account was advocated by MacKeben and Nakayama (1993), who observed a gap effect in subjects who performed a discrimination task without eye movements. On the other hand, the oculo-motor account assumes that the gap effect is owing to premotor programming specific to eye movement (Kingstone & Klein, 1993; Reuter-Lorenz, Hughes, & Fendrich, 1991; Tam & Stelmach, 1993). Which one of these two accounts better explains the gap effect remains an issue of debate. However, the oculo-motor account could not explain the result of MacKeben and Nakayama (1993) since their task did not involve eye movements at all. For this reason, we adopt the attentional explanation to consider the developmental data, as discussed by Hood and Atkinson (1993). According to this 449
450
Matsusawa and Shimoio
view, the gap effect observed in young infants suggests that their attention is disengaged in the gap condition, but they have difficulty disengaging their attention in the overlap condition. The attentional account traditionally assumed only a single process of disengagement either occurs before (in the gap condition) or after (in the overlap condition) the target presentation. However, the developmental difference of disengagement in the gap and overlap conditions seems to require an additional assumption. It would be plausible to assume that the process which lead to the attentional disengagement are different in different trial types, even though the disengagement process itself is single. In this article, the term “gap disengagement” refers to the process that leads to disengagement in the gap condition, which is triggered by the disappearance of a fixation point, and “overlap disengagement” refers to the process that leads to disengagement in the overlap condition, which is facilitated by the appearance of a peripheral target without the disappearance of a fixation point. Therefore, the previous findings could be interpreted, as suggested by Hood and Atkinson (1993), to mean that these two processes of disengagement are based on different mechanisms with different developmental time courses; early maturation of the gap disengagement mechanism and later maturation of the overlap disengagement mechanism, and the latter of which presumably imposes constraints and leads to orientation difficulty in young infants. Basically, this study was a replication of that conducted by Hood and Atkinson (1993), who measured SRTs in the overlap, no-overlap and gap conditions of infants. We, however, have tried to resolve some of the problems, listed below, remained after their study. One problem was that the SRTs of infants were, in general, much longer than those of adults in all the conditions of their study. The consistently longer reaction times, including those in the gap condition, of the former may mean that orientation behavior in infants is constrained by immaturity of the oculo-motor system. This, however, is dubious because the long SRTs might have been caused by the type of stimulus Hood and Atkinson used. They used a schematic face, which was the most attractive stimulus for young infants, as the fixation point and this particular stimulus might have made
them take a long time before they made saccades away. Another possibility is that the gap intervals used (240 and 720 ms) were not optimal for the younger infants. The optimal interval for adults was found to be 200 ms (Fischer, 1986), but that for infants is not known. Thus, in order to examine oculo-motor system maturation, we intended to obtain the shortest possible SRTs by adopting the following methodological modifications: 1.
A less attractive central fixation stimulus and a more attractive target were used.
2.
Visual reinforcement was presented when the infant made a saccade towards the target successfully.
3.
The effects of three gap intervals (200,400, and 800 ms) were compared.
The other problem arising from the study of Hood and Atkinson (1993) was that the difference between the SRTs in the overlap and nooverlap conditions of the oldest infants they tested (6-months-old) was still much greater than that in adults, implying that the overlap disengagement is still immature at 6 months of age. In this study, we tried to establish how and when the overlap disengagement efficiency of infants reaches to the adult level, by studying older infants up to 1 year of age and adults. Five 2.5month-old (M = 11.40 weeks, SD = 9.20 days), six 3.5month-old (M = 16.20 weeks, SD = 10.30 days), seven 4.5-month-old (M = 20.00 weeks, SD = 7.30 days), six 6month-old (M = 26.30 weeks, SD = 11.40 days), six 8-month-old (M = 35.10 weeks, SD = 15.80 days), seven lo-month-old (M = 43.90 weeks, SD = 15.50 days) and eight 12-month-old (M = 53.50 weeks, SD = 23.00 days) infants and five adults (M = 26.00 years, SD = 2.90 years) were tested. Ten of the infants participated in this experiment more than once when they were in different age groups. Seventeen other infants were tested, but their data were not included because they completed less than 20 trials successfully. Each subject was seated at a distance of 57 cm from a 29-in monitor in a semi-dark room. Almost all the infant subjects sat on their mother’s knee, but some young subjects sat in a baby chair in order to keep their posture optimal. The experimenter in the next room monitored
Infants’ Saccades and Attention
the subject’s eye movement by means of a video camera mounted above the monitor and controlled stimulus presentation by a microcomputer (Commodore Amiga 2000). The video images of the eye movements were overlaid synchronously with the presented stimuli and recorded on videotape. White stimuli were presented on a black background. Two types of fixation point and four types of target and reinforcement stimuli were presented in random order across trials. The fixation point subtending a visual angle of 7.5” was presented at the bottom center of the display either as a 2 x 2 brig pattern or a pattern composed of four diamonds. Both patterns rotated 90” 1.5 times per/s with synchronized beep sounds. The target subtending a visual angle of 12” was then presented randomly either at the top left or top right of the display at a distance from the fixation point of approximately 28”. The target was either one of three schematic faces of animals or a dot-textured hexagon. The four types of reinforcement stimulus were of the same pattern as the targets, but they moved in synchrony with melodic music for either 1.5 or 3 s. The experimenter initiated each trial by pressing a key to present a fixation point. When the experimenter judged that the subject was looking at the fixation point, she pressed the key again. One set of the following five conditions was chosen randomly and proceeded by the computer: 1.
overlap
2.
no-overlap
3.
200-ms gap
4.
400-ms gap
5.
800-ms gap
The overlap Condition 1 involved a target appearing while the fixation point remained, whereas for the Conditions 2-5, the fixation point disappeared and a target appeared after an interval, which we call the gap interval, of 2) 0,3) 200, 4) 400 and 5) 800 ms. When the experimenter judged that the subject had made a saccade towards the target, she presented a reinforcement stimulus. When the experimenter judged that the subject had made a saccade else-
451
where than towards the target, she erased the target. When no saccade occurred within three seconds of target presentation, the computer presented a reinforcement stimulus automatically. The inter-trial interval was controlled by the experimenter according to the subject’s state while the display was blank. The experiment was continued until the subject became fuzzy or sleepy. The procedure for adults was the same as that for infants, with the following exceptions: 1.
Each subject performed 200 trials.
2.
Stimulus presentation was controlled matically by the microcomputer.
3.
The subjects were instructed to keep fixating on the fixation point and to make a saccade towards the target as soon as it was presented.
auto-
The eye movements and stimuli recorded on videotape were analyzed. A coder first judged the acceptability of each trial according to the following four criteria: The subject was looking at the location fixation point when the target appeared.
of
The subject did not blink during the time between the disappearance of the fixation point (or appearance of the target in the case of the overlap condition) and the end of the saccade. The subject’s first saccade was from the location of the fixation point towards the target. The subject’s body did not move during the saccade. The mean number of trials completed by all the infant subjects was 78.82 (SD = 20.81) and 50.7% of them were considered to meet these criteria and were accepted. Neither the trial number, F(6, 38) = 1.95, n.s., nor the number of accepted trials, F(6, 38) = 1.85, n.s., differed significantly among the age groups. The blink error (criterion 2) occurred more often under the 400 and 800-ms gap than all the other conditions, x2(4) = 76.40, p < .OOl, as did the directional error (criterion 3), x2(4) = 428.26, p < .OOl, with all the age groups.
452
Matruzawa
The SRTs of the accepted trials in the video frames (1 frame = 33.3 ms) that occurred between the appearance of a target and the onset of a saccade were measured. Initially this analysis was performed by one of authors. Two other graduate students, who were unaware of the purpose of this experiment, analyzed the first 50 trials of two subjects (one was 3 months old and the other, 8 months old), and the correlations between these two coders and the author were high (0.84 to 0.87 correlations for acceptability judgment and 0.90 to 0.99 correlations for the measured SRTs). Saccades with reaction times between 100 and 3000 ms were used to calculate the mean SRTs. SRTs of less than 100 ms were excluded because they were regarded as anticipatory (1.2% for infants and 0.6% for adults), as were those over 3000 ms Sub.N=5
6 7
6
6
7
6
5
120(I-
1OOC I--
60CI--
t
overlap
-O-
no-overlap
4
200-ms-gap
t
400-ms-gap
t
600-ms-gap
-
l--
400 I--
200
0
Note.
,,,I
2.53.54.5
I
I
6 6 10 Age (months)
I
I
12
adults
Although our cross-sectional data may not be appropriate for presenting in the line graph, we adopted it because we thought it would be more suitable to make the developmental change in SRTs in each condition more visible.
Figure 1. Mean SRT under each condition as a function of age. Vertical bars indicate the standard error.
and Shimoio
because they occurred after reinforcement. The percentages of saccades eliminated for this reason were higher for the younger than older age groups, x2(4) = 75.55,~ < .OOl, and in the overlap compared with the other conditions, x2(4) = 75.67, p < .OOl. All the SRTs were transformed logarithmically for analysis. Figure 1 shows the mean SRT as a function of age in each condition. The developmental curve for the overlap condition was extremely steep between 2.5 and 6 months of age, whereas the curve for the 400-ms gap condition was almost flat across all the age groups. Analysis of variance revealed a significant main effect of age group in all the conditions, as shown in Table 1. Subjecting the data for adjacent age groups to the Aspin-Welch test revealed significant differences in the overlap condition among the younger age groups, but not among the older age groups, although the difference between the 12-month-old and adult groups was significant. There were no significant differences between any adjacent age groups in the 400-ms gap condition. However, the failure to obtain statistically significant differences could be due, at least in part, to the relatively small numbers of infants studied. This developmental tendency of the mean SRTs was consistent with the data for eight of the 10 infants who participated in this experiment more than once, when the data were analyzed longitudinally. Table 2 shows effects of the conditions on each age group. Analysis of variance revealed a significant main effect of the conditions on all the age groups. The Aspin-Welch test revealed that the difference between the overlap and nooverlap conditions tended to be significant for the younger, but not the older, age groups. The difference between the no-overlap and 400-ms gap conditions was significant for every age group, but that between the no-overlap and 200ms gap conditions was significant only for the older age groups. The condition under which the shortest mean SRT occurred varied with the age group. The mean SRTs in the 400-ms gap condition of the younger age groups were the shortest, whereas for the oldest infants, the mean SRTs in the 200-ms gap condition was the shortest. Therefore, in comparison with the older infants, the younger infants had difficulty making saccades in the overlap condition, whereas they showed as marked a gap effect as the older
Infants’ Saccades and Attention
453
TABLE 1 Results of ANOVA and Aspin-Welch Test for Effect of Age on SRTs t value of Aspin-Welch Test (only those significant are listed)
ANOVA (main effect of age) Conditions Overlap No-overlap 200-ms gap 400-ms gop 800-ms gap
Age Groups
F
P
2.5 > 3.5
3.5 > 4.5
4.5 > 6
6 > 8
8> 10
10 > 12
12 > Adult
42.25 42.20 59.70 12.88
<.OOl <.OOl <.OOl <.OOl
2.76 3.31 -
2.22 -
3.40 2.45 -
4.82 3.02 -
-2.65 -
5.57 -
3.33 7.78 -
22.31
<.OOl
-
-
-
2.27
-
-
4.89
TABLE 2 Results of ANOVA and Aspin-Welch lest for Effect of Condition on SRTs ANOVA (Main effect of condition)
t value in Aspin-Welch test (only those signhificant are listed)
F
P
overlap > no overlap
2.5 3.5 4.5 6 8 10
14.38 10.68 19.97 11.41 13.76 19.19
C.001 C.001 C.001 C.001 C.001 C.001
4.39 3.43 4.16 3.33 -
2.03 5.70 4.37 6.83
3.98 3.68 4.20 4.85 2.42 6.86
12 Adult
45.96 60.73
<.OOl C.001
7.57
11.11 -
7.31 6.11
Age Groups
subjects (Table 2). This developmental pattern of SRTs was consistent with that observed in the previous study by Hood and Atkinson (1993). However, modifications of the stimuli and gap durations in our study revealed very fast SRTs, much faster than those reported in the previous study, of the youngest infants (Figure 1). The mean SRT in the 400-ms gap condition of the 2.5month-old infants was only about 100 ms longer than that of the adults, indicating these young infants had no difficulty generating saccades when their attention was automatically disengaged by the disappearance of a fixation point. This result suggests that both oculo-motor system and gap disengagement are already mature to an extent by 2.5 months of age. Therefore, the SRT changes in the overlap condition represent development specific to overlap disengagement. In contrast to the slight SRT changes in the 400-ms gap condition (Table l), the mean SRT of the youngest group in the
no-overlap > 200-ms gap
no-overlap > 200-ms gap > 400-ms gap 400-ms gap 4.36 2.70 2.17 -2.25 -
overlap condition was longer than those of the older groups over 600 ms (Figure l), it decreased sharply with age up to 6 months and then changed little up to 1 year of age (Table 1). These results suggest that overlap disengagement changes dramatically during the first 6 months of life, unlike gap disengagement, which seems to develop earlier. Thus, we conclude that the processes which lead to the attentional disengagement are different in different trial types, and that immaturity of the mechanism which underlies the disengagement in the overlap condition is a constraint resulting in orientation difficulty in young infants. This view is consistent with not only our present data but also Hood and Atkinson’s (1993). At around 6 months of age, infants become able to control their orientation behavior qualitatively in the same manner as adults, who can disengage their attention and make saccades towards a peripheral stimulus readily, even when the fixated stimulus does not disappear.
454
Motsuzawa and Shimoio
Our data are consistent with the neurological hypothesis that the development of orientation behavior is restricted by the maturational states of distinct oculo-motor pathways in the brain. Early development of gap disengagement reflects early maturation of the pathway from the retina to the superior colliculus (Hood & Atkinson, 1993), whereas the later development of overlap disengagement reflects slow maturation of higher cortical pathways, including the frontal eye fields and parietal lobe (Hood & Atkinson, 1993; Johnson, 1990; Johnson et al., 1991). Another finding of this study was that the gap effect did not occur in the 200-ms gap condition in the younger infants (Table 2), although 200 ms was the optimal gap interval for adults (Fischer & Weber, 1993), and the oldest infants participating in our study. This indicates that gap disengagement by younger infants takes longer in comparison with older infants and adults. The mechanisms underlying gap disengagement may become more efficient gradually during the 1st year of life.’ We assumed that the gap effect is attentional in nature, as suggested by Fischer and his colleagues (Fischer, 1986; Fischer & Breitmeyer, 1987; Fischer & Weber, 1993) and MacKeben and Nakayama (1993). As mentioned before, however, there is an alternative, oculo-motor account of the gap effect (Kingstone & Klein, 1993; Reuter-Lorenz, Hughes, & Fendrich, 1991; Tam & Stelmach, 1993). Thus some researchers may still prefer to characterize the fast saccades in the gap condition observed in younger infants as early maturation of pre-motor programming specific to eye movement, rather than of attentional disengagement. In that case, however, they need to further explain why the SRTs in the overlap condition in younger infants were so slow. Our conclusion that overlap disengagement develops later than gap disengagement raises a question about visual acuity, which has been measured using a preferential looking paradigm (Dobson & Teller, 1978; Mayer & Dobwhich typically involves son, 1982), measuring visual acuity with the fixation point remaining (i.e., in the overlap condition). This problem is addressed in Atkinson et al. (1988, 1992).
FOOTNOTE 1.
It could be argued that the reduction of the optimal gap duration observed in the older infants may simply have reflected frequent anticipatory responses. We consider this interpretation seems unlikely because if this were the case, the older infants, who showed the shortest SRTs in the 200-ms gap condition, would have produced more saccades in the wrong direction in the 200ms gap condition than the 400-ms gap or any other conditions and the opposite results were obtained. The rate of saccades in the wrong direction of the oldest infants in the 200-ms gap condition was 6%, which was smaller than that in the 400-ms gap condition (15%). This was the same tendency as of the youngest group (4% and 15% in the 200- and 400-ms gap conditions respectively). Moreover, very few saccades occurring after target presentation were observed to be in the wrong direction in all the conditions and for all the age groups. These results together indicate that there was very little effect of anticipatory saccades, if any. AUTHORS’
NOTES
This research has been supported by a Grant-inAid for Scientific Research on Priority Areas from MESC, Japan. REFERENCES Aslin, R. N., & Salapatek, P. (1975). Saccadic localization of visual targets by the very young human infant. Perception and Psychophysics, 17,293-302. Atkinson, J., Hood, B., Braddick, 0. J., & WattamBell, J. (1988). Infants’ control of fixation shifts with single and competing targets: Mechanisms of shifting attention. Perception, 17,367-368. Atkinson, J., Hood, B., Wattam-Bell, J., & Braddick, 0. (1992). Changes in infants’ ability to switch visual attention in the first three months of life. Perception, 21,643-653. Dobson, V., & Teller, D. Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research, 18, 1469-1483. Fischer, B. (1986). The role of attention in the preparation of visually guided eye movements in
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monkey and man. Psychological Research, 48, 25 l-257. Fischer, B., & Breitmeyer, B. (1987). Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychalogia, 25.73-83. Fischer, B., & Weber, H. (1993). Express saccades and visual attention. Behavioral and Brain Sciences, 16,553-610. Hood, B. M., & Atkinson, J. (1993). Disengaging visual attention in the infant and adult. Infant Behavior and Development, 16,405422. Johnson, M. H. (1990). Cortical maturation and the development of visual attention in early infancy. Journal of Cognitive Neuroscience, 2, 81-95. Johnson, M. H., Posner, M. I., & Rothbart, M. K. (1991). Components of visual orienting in early infancy: Contingency learning, anticipatory looking, and disengaging. Journal of Cognitive Neuroscience, 3, 335-344. Kingstone, A., & Klein, R. M. (1993). Visual offsets facilitate saccadic latency: Does predisengagement of visuospatial attention mediate this gap
effect? Journal of Experimental Psychology: Human Perception and Peflormance, 19, 1251-1265. MacKeben, M., & Nakayama, K. (1993). Express attentional shifts. Vision Research, 33,85-90. Mayer, D. L., & Dobson, V. (1982). Visual acuity development in infants and young children, as assessed by operant preferential looking. Vision Research, 22, 1141-1151. Reuter-Lorenz, P. A., Hughes, H. C., & Fendrich, R. (1991). The reduction of saccadic latency by prior offset of the fixation point: .An analysis of the gap effect. Perception and Psychophysics, 49, 167-175. Tam, W. J., & Stelmach, L. B. (1993). Viewing behavior: Ocular and attentional disengagement. Perception and Psychophysics, 54,21 l222.
19 June 1996;
Revised
15 January
1997
W
pp. 449-455
ISSN 0163-6383 All rights of reproduction in any form resewed.
Infants’ Fast Saccades in the Gap Paradigm and Development of Visual Attention MASAKO
MATSUZAWA
Shirayuri College
SHINSUKE
SHIMOJO
University of Tokyo The
saccadic reaction times (SRTs) in the overlap, no-overlap, and gap conditions of 2.5- to 12-month-old infants and adults were measured. In the overlap condition, the SRTs of younger infants were over 600 ms longer than those of older infants, whereas the SRTs in the gap condition of the younger infants were 300-350 ms, much faster than reported hitherto, and were shortened only by about 100 ms. The results indicate that the oculo-motor system and attention process for disengagement in the gap condition mature earlier than the attention process for disengagement in the overlap condition.
saccades
eye movements
reaction
times
Infants of a few months of age have difficulty orienting towards peripheral stimuli. Studies in which saccadic reaction times (SRTs) were measured demonstrated that the SRTs were longer in “overlap” than “no-overlap” condition and this tendency was more pronounced in the younger infants (Aslin & Salapatek, 1975; Johnson, Posner, & Rothbart, 1991). In the overlap condition, a fixation point remained after presentation of a peripheral target, whereas in the no-overlap condition, a fixation point disappeared upon presentation of a peripheral target. Therefore, the results (i.e., the difference between the SRTs in the overlap and no-overlap conditions of young infants), suggest that a critical factor responsible for the orientation difficulty of young infants is the inability to disengage their attention from a currently fixated stimulus (Johnson, 1990; Johnson et al., 1991). This suggestion is supported by the studies of Atkinson, Hood, Braddick, and Wattam-Bell (1988) and Atkinson, Hood, WattamBell, and Braddick (1992), who found the same pattern of results and eliminated the possibility that the effect was confounded with developmental changes in visual sensitivity by adjusting the luminance thresholds for the different age groups. More recently, Hood and Atkinson (1993) measured SRTs in “gap” condition as well as the Direct all correspondence to Masako Matsuzawa, Department of Developmental Psychology, Shirayuri College, 1-25 Midorigaoka, Chofu-shi, Tokyo 182, Japan.
aaa effect
visual attention
infants
overlap and no-overlap conditions. In the gap condition, a fixation point disappeared before the delayed presentation of a peripheral target. The SRTs in the gap condition of both younger and older infants were shorter than those in the no-overlap condition. The gap effect has been explained in two ways in studies using adults or animals-by an attentional account or an oculomotor one. The former assumes that the gap effect occurs because the attention on a fixation point is disengaged automatically by the disappearance of the fixation point in the gap condition. The disengagement of attention occurs prior to target presentation, thus makes the SRTs shorter (Fischer, 1986; Fischer & Breitmeyer, 1987; Fischer & Weber, 1993). This attentional account was advocated by MacKeben and Nakayama (1993), who observed a gap effect in subjects who performed a discrimination task without eye movements. On the other hand, the oculo-motor account assumes that the gap effect is owing to premotor programming specific to eye movement (Kingstone & Klein, 1993; Reuter-Lorenz, Hughes, & Fendrich, 1991; Tam & Stelmach, 1993). Which one of these two accounts better explains the gap effect remains an issue of debate. However, the oculo-motor account could not explain the result of MacKeben and Nakayama (1993) since their task did not involve eye movements at all. For this reason, we adopt the attentional explanation to consider the developmental data, as discussed by Hood and Atkinson (1993). According to this 449
450
Matsusawa and Shimoio
view, the gap effect observed in young infants suggests that their attention is disengaged in the gap condition, but they have difficulty disengaging their attention in the overlap condition. The attentional account traditionally assumed only a single process of disengagement either occurs before (in the gap condition) or after (in the overlap condition) the target presentation. However, the developmental difference of disengagement in the gap and overlap conditions seems to require an additional assumption. It would be plausible to assume that the process which lead to the attentional disengagement are different in different trial types, even though the disengagement process itself is single. In this article, the term “gap disengagement” refers to the process that leads to disengagement in the gap condition, which is triggered by the disappearance of a fixation point, and “overlap disengagement” refers to the process that leads to disengagement in the overlap condition, which is facilitated by the appearance of a peripheral target without the disappearance of a fixation point. Therefore, the previous findings could be interpreted, as suggested by Hood and Atkinson (1993), to mean that these two processes of disengagement are based on different mechanisms with different developmental time courses; early maturation of the gap disengagement mechanism and later maturation of the overlap disengagement mechanism, and the latter of which presumably imposes constraints and leads to orientation difficulty in young infants. Basically, this study was a replication of that conducted by Hood and Atkinson (1993), who measured SRTs in the overlap, no-overlap and gap conditions of infants. We, however, have tried to resolve some of the problems, listed below, remained after their study. One problem was that the SRTs of infants were, in general, much longer than those of adults in all the conditions of their study. The consistently longer reaction times, including those in the gap condition, of the former may mean that orientation behavior in infants is constrained by immaturity of the oculo-motor system. This, however, is dubious because the long SRTs might have been caused by the type of stimulus Hood and Atkinson used. They used a schematic face, which was the most attractive stimulus for young infants, as the fixation point and this particular stimulus might have made
them take a long time before they made saccades away. Another possibility is that the gap intervals used (240 and 720 ms) were not optimal for the younger infants. The optimal interval for adults was found to be 200 ms (Fischer, 1986), but that for infants is not known. Thus, in order to examine oculo-motor system maturation, we intended to obtain the shortest possible SRTs by adopting the following methodological modifications: 1.
A less attractive central fixation stimulus and a more attractive target were used.
2.
Visual reinforcement was presented when the infant made a saccade towards the target successfully.
3.
The effects of three gap intervals (200,400, and 800 ms) were compared.
The other problem arising from the study of Hood and Atkinson (1993) was that the difference between the SRTs in the overlap and nooverlap conditions of the oldest infants they tested (6-months-old) was still much greater than that in adults, implying that the overlap disengagement is still immature at 6 months of age. In this study, we tried to establish how and when the overlap disengagement efficiency of infants reaches to the adult level, by studying older infants up to 1 year of age and adults. Five 2.5month-old (M = 11.40 weeks, SD = 9.20 days), six 3.5month-old (M = 16.20 weeks, SD = 10.30 days), seven 4.5-month-old (M = 20.00 weeks, SD = 7.30 days), six 6month-old (M = 26.30 weeks, SD = 11.40 days), six 8-month-old (M = 35.10 weeks, SD = 15.80 days), seven lo-month-old (M = 43.90 weeks, SD = 15.50 days) and eight 12-month-old (M = 53.50 weeks, SD = 23.00 days) infants and five adults (M = 26.00 years, SD = 2.90 years) were tested. Ten of the infants participated in this experiment more than once when they were in different age groups. Seventeen other infants were tested, but their data were not included because they completed less than 20 trials successfully. Each subject was seated at a distance of 57 cm from a 29-in monitor in a semi-dark room. Almost all the infant subjects sat on their mother’s knee, but some young subjects sat in a baby chair in order to keep their posture optimal. The experimenter in the next room monitored
Infants’ Saccades and Attention
the subject’s eye movement by means of a video camera mounted above the monitor and controlled stimulus presentation by a microcomputer (Commodore Amiga 2000). The video images of the eye movements were overlaid synchronously with the presented stimuli and recorded on videotape. White stimuli were presented on a black background. Two types of fixation point and four types of target and reinforcement stimuli were presented in random order across trials. The fixation point subtending a visual angle of 7.5” was presented at the bottom center of the display either as a 2 x 2 brig pattern or a pattern composed of four diamonds. Both patterns rotated 90” 1.5 times per/s with synchronized beep sounds. The target subtending a visual angle of 12” was then presented randomly either at the top left or top right of the display at a distance from the fixation point of approximately 28”. The target was either one of three schematic faces of animals or a dot-textured hexagon. The four types of reinforcement stimulus were of the same pattern as the targets, but they moved in synchrony with melodic music for either 1.5 or 3 s. The experimenter initiated each trial by pressing a key to present a fixation point. When the experimenter judged that the subject was looking at the fixation point, she pressed the key again. One set of the following five conditions was chosen randomly and proceeded by the computer: 1.
overlap
2.
no-overlap
3.
200-ms gap
4.
400-ms gap
5.
800-ms gap
The overlap Condition 1 involved a target appearing while the fixation point remained, whereas for the Conditions 2-5, the fixation point disappeared and a target appeared after an interval, which we call the gap interval, of 2) 0,3) 200, 4) 400 and 5) 800 ms. When the experimenter judged that the subject had made a saccade towards the target, she presented a reinforcement stimulus. When the experimenter judged that the subject had made a saccade else-
451
where than towards the target, she erased the target. When no saccade occurred within three seconds of target presentation, the computer presented a reinforcement stimulus automatically. The inter-trial interval was controlled by the experimenter according to the subject’s state while the display was blank. The experiment was continued until the subject became fuzzy or sleepy. The procedure for adults was the same as that for infants, with the following exceptions: 1.
Each subject performed 200 trials.
2.
Stimulus presentation was controlled matically by the microcomputer.
3.
The subjects were instructed to keep fixating on the fixation point and to make a saccade towards the target as soon as it was presented.
auto-
The eye movements and stimuli recorded on videotape were analyzed. A coder first judged the acceptability of each trial according to the following four criteria: The subject was looking at the location fixation point when the target appeared.
of
The subject did not blink during the time between the disappearance of the fixation point (or appearance of the target in the case of the overlap condition) and the end of the saccade. The subject’s first saccade was from the location of the fixation point towards the target. The subject’s body did not move during the saccade. The mean number of trials completed by all the infant subjects was 78.82 (SD = 20.81) and 50.7% of them were considered to meet these criteria and were accepted. Neither the trial number, F(6, 38) = 1.95, n.s., nor the number of accepted trials, F(6, 38) = 1.85, n.s., differed significantly among the age groups. The blink error (criterion 2) occurred more often under the 400 and 800-ms gap than all the other conditions, x2(4) = 76.40, p < .OOl, as did the directional error (criterion 3), x2(4) = 428.26, p < .OOl, with all the age groups.
452
Matruzawa
The SRTs of the accepted trials in the video frames (1 frame = 33.3 ms) that occurred between the appearance of a target and the onset of a saccade were measured. Initially this analysis was performed by one of authors. Two other graduate students, who were unaware of the purpose of this experiment, analyzed the first 50 trials of two subjects (one was 3 months old and the other, 8 months old), and the correlations between these two coders and the author were high (0.84 to 0.87 correlations for acceptability judgment and 0.90 to 0.99 correlations for the measured SRTs). Saccades with reaction times between 100 and 3000 ms were used to calculate the mean SRTs. SRTs of less than 100 ms were excluded because they were regarded as anticipatory (1.2% for infants and 0.6% for adults), as were those over 3000 ms Sub.N=5
6 7
6
6
7
6
5
120(I-
1OOC I--
60CI--
t
overlap
-O-
no-overlap
4
200-ms-gap
t
400-ms-gap
t
600-ms-gap
-
l--
400 I--
200
0
Note.
,,,I
2.53.54.5
I
I
6 6 10 Age (months)
I
I
12
adults
Although our cross-sectional data may not be appropriate for presenting in the line graph, we adopted it because we thought it would be more suitable to make the developmental change in SRTs in each condition more visible.
Figure 1. Mean SRT under each condition as a function of age. Vertical bars indicate the standard error.
and Shimoio
because they occurred after reinforcement. The percentages of saccades eliminated for this reason were higher for the younger than older age groups, x2(4) = 75.55,~ < .OOl, and in the overlap compared with the other conditions, x2(4) = 75.67, p < .OOl. All the SRTs were transformed logarithmically for analysis. Figure 1 shows the mean SRT as a function of age in each condition. The developmental curve for the overlap condition was extremely steep between 2.5 and 6 months of age, whereas the curve for the 400-ms gap condition was almost flat across all the age groups. Analysis of variance revealed a significant main effect of age group in all the conditions, as shown in Table 1. Subjecting the data for adjacent age groups to the Aspin-Welch test revealed significant differences in the overlap condition among the younger age groups, but not among the older age groups, although the difference between the 12-month-old and adult groups was significant. There were no significant differences between any adjacent age groups in the 400-ms gap condition. However, the failure to obtain statistically significant differences could be due, at least in part, to the relatively small numbers of infants studied. This developmental tendency of the mean SRTs was consistent with the data for eight of the 10 infants who participated in this experiment more than once, when the data were analyzed longitudinally. Table 2 shows effects of the conditions on each age group. Analysis of variance revealed a significant main effect of the conditions on all the age groups. The Aspin-Welch test revealed that the difference between the overlap and nooverlap conditions tended to be significant for the younger, but not the older, age groups. The difference between the no-overlap and 400-ms gap conditions was significant for every age group, but that between the no-overlap and 200ms gap conditions was significant only for the older age groups. The condition under which the shortest mean SRT occurred varied with the age group. The mean SRTs in the 400-ms gap condition of the younger age groups were the shortest, whereas for the oldest infants, the mean SRTs in the 200-ms gap condition was the shortest. Therefore, in comparison with the older infants, the younger infants had difficulty making saccades in the overlap condition, whereas they showed as marked a gap effect as the older
Infants’ Saccades and Attention
453
TABLE 1 Results of ANOVA and Aspin-Welch Test for Effect of Age on SRTs t value of Aspin-Welch Test (only those significant are listed)
ANOVA (main effect of age) Conditions Overlap No-overlap 200-ms gap 400-ms gop 800-ms gap
Age Groups
F
P
2.5 > 3.5
3.5 > 4.5
4.5 > 6
6 > 8
8> 10
10 > 12
12 > Adult
42.25 42.20 59.70 12.88
<.OOl <.OOl <.OOl <.OOl
2.76 3.31 -
2.22 -
3.40 2.45 -
4.82 3.02 -
-2.65 -
5.57 -
3.33 7.78 -
22.31
<.OOl
-
-
-
2.27
-
-
4.89
TABLE 2 Results of ANOVA and Aspin-Welch lest for Effect of Condition on SRTs ANOVA (Main effect of condition)
t value in Aspin-Welch test (only those signhificant are listed)
F
P
overlap > no overlap
2.5 3.5 4.5 6 8 10
14.38 10.68 19.97 11.41 13.76 19.19
C.001 C.001 C.001 C.001 C.001 C.001
4.39 3.43 4.16 3.33 -
2.03 5.70 4.37 6.83
3.98 3.68 4.20 4.85 2.42 6.86
12 Adult
45.96 60.73
<.OOl C.001
7.57
11.11 -
7.31 6.11
Age Groups
subjects (Table 2). This developmental pattern of SRTs was consistent with that observed in the previous study by Hood and Atkinson (1993). However, modifications of the stimuli and gap durations in our study revealed very fast SRTs, much faster than those reported in the previous study, of the youngest infants (Figure 1). The mean SRT in the 400-ms gap condition of the 2.5month-old infants was only about 100 ms longer than that of the adults, indicating these young infants had no difficulty generating saccades when their attention was automatically disengaged by the disappearance of a fixation point. This result suggests that both oculo-motor system and gap disengagement are already mature to an extent by 2.5 months of age. Therefore, the SRT changes in the overlap condition represent development specific to overlap disengagement. In contrast to the slight SRT changes in the 400-ms gap condition (Table l), the mean SRT of the youngest group in the
no-overlap > 200-ms gap
no-overlap > 200-ms gap > 400-ms gap 400-ms gap 4.36 2.70 2.17 -2.25 -
overlap condition was longer than those of the older groups over 600 ms (Figure l), it decreased sharply with age up to 6 months and then changed little up to 1 year of age (Table 1). These results suggest that overlap disengagement changes dramatically during the first 6 months of life, unlike gap disengagement, which seems to develop earlier. Thus, we conclude that the processes which lead to the attentional disengagement are different in different trial types, and that immaturity of the mechanism which underlies the disengagement in the overlap condition is a constraint resulting in orientation difficulty in young infants. This view is consistent with not only our present data but also Hood and Atkinson’s (1993). At around 6 months of age, infants become able to control their orientation behavior qualitatively in the same manner as adults, who can disengage their attention and make saccades towards a peripheral stimulus readily, even when the fixated stimulus does not disappear.
454
Motsuzawa and Shimoio
Our data are consistent with the neurological hypothesis that the development of orientation behavior is restricted by the maturational states of distinct oculo-motor pathways in the brain. Early development of gap disengagement reflects early maturation of the pathway from the retina to the superior colliculus (Hood & Atkinson, 1993), whereas the later development of overlap disengagement reflects slow maturation of higher cortical pathways, including the frontal eye fields and parietal lobe (Hood & Atkinson, 1993; Johnson, 1990; Johnson et al., 1991). Another finding of this study was that the gap effect did not occur in the 200-ms gap condition in the younger infants (Table 2), although 200 ms was the optimal gap interval for adults (Fischer & Weber, 1993), and the oldest infants participating in our study. This indicates that gap disengagement by younger infants takes longer in comparison with older infants and adults. The mechanisms underlying gap disengagement may become more efficient gradually during the 1st year of life.’ We assumed that the gap effect is attentional in nature, as suggested by Fischer and his colleagues (Fischer, 1986; Fischer & Breitmeyer, 1987; Fischer & Weber, 1993) and MacKeben and Nakayama (1993). As mentioned before, however, there is an alternative, oculo-motor account of the gap effect (Kingstone & Klein, 1993; Reuter-Lorenz, Hughes, & Fendrich, 1991; Tam & Stelmach, 1993). Thus some researchers may still prefer to characterize the fast saccades in the gap condition observed in younger infants as early maturation of pre-motor programming specific to eye movement, rather than of attentional disengagement. In that case, however, they need to further explain why the SRTs in the overlap condition in younger infants were so slow. Our conclusion that overlap disengagement develops later than gap disengagement raises a question about visual acuity, which has been measured using a preferential looking paradigm (Dobson & Teller, 1978; Mayer & Dobwhich typically involves son, 1982), measuring visual acuity with the fixation point remaining (i.e., in the overlap condition). This problem is addressed in Atkinson et al. (1988, 1992).
FOOTNOTE 1.
It could be argued that the reduction of the optimal gap duration observed in the older infants may simply have reflected frequent anticipatory responses. We consider this interpretation seems unlikely because if this were the case, the older infants, who showed the shortest SRTs in the 200-ms gap condition, would have produced more saccades in the wrong direction in the 200ms gap condition than the 400-ms gap or any other conditions and the opposite results were obtained. The rate of saccades in the wrong direction of the oldest infants in the 200-ms gap condition was 6%, which was smaller than that in the 400-ms gap condition (15%). This was the same tendency as of the youngest group (4% and 15% in the 200- and 400-ms gap conditions respectively). Moreover, very few saccades occurring after target presentation were observed to be in the wrong direction in all the conditions and for all the age groups. These results together indicate that there was very little effect of anticipatory saccades, if any. AUTHORS’
NOTES
This research has been supported by a Grant-inAid for Scientific Research on Priority Areas from MESC, Japan. REFERENCES Aslin, R. N., & Salapatek, P. (1975). Saccadic localization of visual targets by the very young human infant. Perception and Psychophysics, 17,293-302. Atkinson, J., Hood, B., Braddick, 0. J., & WattamBell, J. (1988). Infants’ control of fixation shifts with single and competing targets: Mechanisms of shifting attention. Perception, 17,367-368. Atkinson, J., Hood, B., Wattam-Bell, J., & Braddick, 0. (1992). Changes in infants’ ability to switch visual attention in the first three months of life. Perception, 21,643-653. Dobson, V., & Teller, D. Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research, 18, 1469-1483. Fischer, B. (1986). The role of attention in the preparation of visually guided eye movements in
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monkey and man. Psychological Research, 48, 25 l-257. Fischer, B., & Breitmeyer, B. (1987). Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychalogia, 25.73-83. Fischer, B., & Weber, H. (1993). Express saccades and visual attention. Behavioral and Brain Sciences, 16,553-610. Hood, B. M., & Atkinson, J. (1993). Disengaging visual attention in the infant and adult. Infant Behavior and Development, 16,405422. Johnson, M. H. (1990). Cortical maturation and the development of visual attention in early infancy. Journal of Cognitive Neuroscience, 2, 81-95. Johnson, M. H., Posner, M. I., & Rothbart, M. K. (1991). Components of visual orienting in early infancy: Contingency learning, anticipatory looking, and disengaging. Journal of Cognitive Neuroscience, 3, 335-344. Kingstone, A., & Klein, R. M. (1993). Visual offsets facilitate saccadic latency: Does predisengagement of visuospatial attention mediate this gap
effect? Journal of Experimental Psychology: Human Perception and Peflormance, 19, 1251-1265. MacKeben, M., & Nakayama, K. (1993). Express attentional shifts. Vision Research, 33,85-90. Mayer, D. L., & Dobson, V. (1982). Visual acuity development in infants and young children, as assessed by operant preferential looking. Vision Research, 22, 1141-1151. Reuter-Lorenz, P. A., Hughes, H. C., & Fendrich, R. (1991). The reduction of saccadic latency by prior offset of the fixation point: .An analysis of the gap effect. Perception and Psychophysics, 49, 167-175. Tam, W. J., & Stelmach, L. B. (1993). Viewing behavior: Ocular and attentional disengagement. Perception and Psychophysics, 54,21 l222.
19 June 1996;
Revised
15 January
1997
W