University of Groningen Through the Eyes of an Infant …Infant attention patterns have been reported to be related to later intellectual functioning (see e.g., Colombo, 1993; Yarrow,

University of Groningen

Through the Eyes of an InfantHunnius, S.

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Chapter 5

A Longitudinal Study of Shifts of Attention and Gaze in Preterm and Full-term Infants

AbstractThe development of shifts of attention and gaze was examined, between 6 and 26 weeks corrected age, in full-term and preterm infants. Infants carried out a gaze shifting task with competition and non-competition trials. A video of the infant’s mother’s face and an abstract video appeared as central or peripheral stimulus, which resulted in four different combinations (face-face, face-abstract, abstract-face, abstract-abstract). Until 18 weeks, the preterm infants were quicker in shifting gaze from fixation than full-terms. There were, however, no differences in gaze shifting frequency between preterms and full-terms. At the same time, preterm infants also showed less mature gaze shifting behavior: At the age of 6 weeks, they continued to stare at the location of the central stimulus after the peripheral target had appeared more often than full-terms. Preterms as well as full-terms were more likely to shift gaze away from a face to an abstract peripheral target, while they moved their gaze least frequently and more slowly in the opposite condition (abstract-face). However, there were indi-cations that looking away from an abstract stimulus formed a particular challenge for the preterm infants.

This chapter is based on: Hunnius, S., Geuze, R. H., Bos, A. F., & Zweens, M. J. (submitted for publication). A longitudinal study of shifts of attention and gaze in preterm and full-term infants.

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Pre- and Full-term Infants’ Shifts of Attention and Gaze

INTRODUCTIONThe Development of Attention

During the first few months of life, infants learn a lot about the world around them as they explore it visually. Effective visual exploration, however, requires being able to shift gaze flexibly across different locations. Also during early face-to-face interaction, being able to shift gaze to and away from another person plays a crucial role and thus is important for the social-emotional development of an infant. The attentional skills that allow the infant to strike balance between engaging and shift-ing attention develop during the first few months of life. While the sensory-motor processes involved in detecting and shifting gaze to visual targets are functional after 40 weeks gestational age (Butcher, Kalverboer, & Geuze, 2000), infants between 1 and 4 months of age have difficulty disengaging their attention and gaze from an object or stimulus they are currently fixating (Harris & MacFarlane, 1974; Aslin & Salapatek, 1975). This phenomenon of “obligatory attention” (Stechler & Latz, 1966) or “sticky fixation” (Hood, 1995) can be observed in situations of the daily life, such as social interaction (Kaye & Fogel, 1980), but also in a laboratory context during ha-bituation (Hood, Murray, King, Hooper, Atkinson, & Braddick, 1996) or gaze shifting tasks (Matsuzawa & Shimojo, 1997; Hood & Atkinson, 1993). However, around 5 to 6 months of age, infants’ visual behavior is qualitatively similar to that of adults (Hood & Atkinson, 1993; Matsuzawa & Shimojo, 1997).

Visual Development in Preterm InfantsIt has been reported that visual and attentional development is different in preterm

infants and that preterm infants process visual information differently from full-term infants. Studies on habituation demonstrate that preterm infants exhibit longer look durations than full-terms (see e.g., Rose, Feldman, McCarton, & Wolfson, 1988; Spun-gen, Kurtzberg, & Vaughan, 1985; Sigman, Cohen, Beckwith, & Parmelee, 1986; but: Bonin, Pomerleau, & Malcuit, 1998). But preterm infants do not only need more time to process and habituate to stimuli, they also show lower novelty preference scores when confronted with a familiar and a novel stimulus (Sigman, 1983). In a study by Rose, Gottfried, and Bridger (1979), full-term infants discriminated between a familiar and a novel stimulus at 6 and 12 months, whereas preterms did so only at 12 months of age. This suggests that preterm infants also exhibit deficits concerning their visual recognition memory (Rose et al., 1988; Rose et al., 2001). These observations were found to persist throughout the first year of life (Rose, Feldman, & Jankowski, 2001). Preterm infants have also been shown to spend more time off-task (Rose et al., 1988). During free play alone or with their mothers, high-risk preterm infants of 6 months of age shift their gaze less frequently and notice fewer toys (Landry & Chapieski, 1988).

Consistent with these descriptions of preterms’ less efficient performance, Fried-man, Jacobs, and Werthmann (1981) put forward the position that the visual system of the preterm infant may suffer by the premature exposure to visual input and to the

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extrauterine environment. However, in the literature on preterm infants conflicting evidence of both delayed and advanced visual development can be found. Preterm infants are reported to show precocious maturity when focusing and when tracking moving stimuli (Dubowitz, Dubowitz, Morante, & Verghote, 1980; Bloch, 1983). Fielder, Foreman, Moseley, and Robinson (1993) thus suggest that preterms with few medical problems might benefit from early visual experience.

Infant attention patterns have been reported to be related to later intellectual functioning (see e.g., Colombo, 1993; Yarrow, Klein, Lomonaco, & Morgan, 1975; Fagan & McGrath, 1981), and this connection has been described for preterm infants as well (Cohen & Parmelee, 1983; Sigman et al., 1986). Preterm infants have been shown to be at risk for problems concerning their intellectual and attentional functioning in later childhood (Breslau & Chilcoat, 2000; Anderson et al., 2003). This underlines the importance of examining the development of attention closely and exploring possible early differences between high-risk infants and healthy controls.

Shifts of Gaze in Preterm InfantsThere are several studies which have compared full- and preterm infants’ local-

ization of stimuli. Tasks which examine these simple shifts of gaze first attract the infant’s gaze to a fixation point. Then this central fixation stimulus is extinguished as a new target appears in the periphery. The frequency and latency of the infant’s localization of the peripheral stimulus is assessed and provides information on the infant’s sensory-motor processing.

Several studies have shown that preterm infants are more efficient in shifting their gaze as they moved their gaze to a peripheral target more frequently (Butcher, Kalverboer, Geuze, & Stremmelaar, 2002) and with shorter latencies (Foreman, Fielder, Price, & Bowler, 1991; Atkinson, 2000; Butcher et al., 2002) than their full-terms age mates. However, these studies also demonstrated that the gain from early visual ex-perience was only temporary. When infants were older than 4 to 6 weeks of corrected age, pre- and full-terms’ gaze shifting behavior was about equally efficient (Foreman et al., 1991; Butcher et al., 2002; Atkinson, 2000). Preterm infants with more severe medical complications did not substantially benefit (Butcher et al., 2002) or performed even more poorly than full-terms (Landry, Leslie, Fletcher, & Francis, 1985). On the other hand, there are also studies which describe low-risk preterm infants being less efficient in their gaze shifting behavior (Friedman, et al., 1981; Masi & Scott, 1983; Vervloed, 1995).

Shifts of Gaze from an Attended Stimulus (Disengagement) in Preterm InfantsThe results of studies addressing the development of gaze shifts away from an

attended stimulus in preterm infants are also rather inconsistent. Disengagement is investigated using tasks in which a fixation stimulus is first presented in the central visual field of the infant, before a target in the periphery is added. In order to look

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away from the persisting stimulus in the center and shift gaze to the periphery, in-fants have to disengage their attention and gaze. Such tasks thus measure both the attentional processes required for disengagement and the sensory-motor processing which is necessary to carry out and eye movement to the competing stimulus in the periphery.

We know of only two studies that examined disengagement of attention in pre- and full-term infants by means of such a specifically designed task. Butcher et al. (2002) studied the development of simple gaze shifts and disengagement in high- and low-risk preterm infants and full-term controls. They reported that low-risk preterms were faster than their full-term age mates in disengaging their attention and gaze during the first 10 weeks after the term date, but lagged behind from 16 weeks on and were significantly slower by 6 months. However, there were no significant differences in disengagement latency between high-risk preterms and full-terms. Concerning the frequency of gaze shifts, the three groups did not differ, but staring behavior persisted slightly longer in the preterm groups. Atkinson (2000) also found shorter latencies of gaze shifts in 4- to 5-week old in relatively healthy preterms. However, Butcher et al. (2002) and Atkinson (2000) interpret their results in relation with their findings on simple gaze shifting: As they also found shorter latencies of simple shifts of gaze, they suggest that disengagement latencies might be shorter in preterm infants due to faster sensory-motor processing. The authors accordingly conclude that mainly early developing sensory and motor processes benefited from early visual experience, but not the later maturing attentional processes.

The Underlying Mechanisms of Disengagement of Attention in InfancyResearchers have explained the disengagement difficulty during early infancy in

different ways. Rothbart, Posner, and Rosicky (1994) suppose that gaze shifts are pre-ceded by a covert shift of attention and accordingly explain disengagement difficulty as problems shifting attention covertly. Johnson (1990) on the other hand, suggests that obligatory attention reflects the inability to generate an eye movement to a pe-ripheral target while processing a stimulus in the central visual field. According to Hood (1995), however, disengagement difficulty is caused by problems breaking gaze from fixation.

Previous studies have shown that the characteristics of the stimuli used in a dis-engagement task influence the infants’ gaze shifting behavior. Both, the stimulus currently under attention and the stimulus in the peripheral visual field affect the frequency and latency of looks to the periphery, and this influence has been shown to change with age (see Chapter 3; Butcher et al., 2000). Whether and how quickly infants carry out gaze shifts is influenced by the physical salience of the stimuli (Finlay & Ivinskis, 1984; Tronick, 1972), but also by higher level attributes of the stimuli such as social meaningfulness (see Chapter 3).

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Aims of the StudyThe results reported in the literature on gaze and attention shifting in pre- and

full-term infants are far from being exhaustive and consistent. The aim of this study thus was to compare the development of disengagement and simple gaze shifts in preterm and full-term infants.

As both simple gaze shifts and disengagement were examined, an experiment with non-competition and competition tasks was created. In a non-competition situation simple shifts of gaze are studied, elicited by a central and a peripheral stimulus, which are presented successively. In the competition condition, on the other hand, the central stimulus persists after the peripheral one appears, and the infant has to disengage his or her attention first, before the gaze can be shifted to the periphery.

As fundamental gaze and attention shifting mechanisms are known to develop during the first few months after the term date, the infant participants of this study were followed between 6 and 26 weeks of (corrected) age. An intense longitudinal design with 6 measurement points was chosen. Young infants – and especially infants with diverse medical histories – tend to differ considerably in their performance on visual tasks. A longitudinal design, however, reduces the inter-individual variance between measurement points and increases the power.

Earlier research has shown that the sort of stimuli used influenced the gaze shift-ing behavior in a disengagement task. Infants shifted their gaze less frequently and more slowly when looking away from an abstract stimulus to a face in the periphery than in the opposite condition (see Chapter 3). Preterm infants, however, have been shown to be visually less responsive to faces than their full-term age mates. They look less at their mother’s (Field, 1977, 1979; Barratt, Roach, & Leavitt, 1992) and a stranger’s face (Masi & Scott, 1983) and are slower in orienting toward those faces (Masi & Scott, 1983). It was thus the second goal of this study to investigate the infants’ gaze shift-ing between different stimuli and explore whether the influence of the stimuli was different in preterm than in full-term infants.

METHODParticipants

Twenty full-term infants (12 girls; 8 boys) and ten preterm infants (4 girls; 6 boys) participated in the longitudinal study. The parents of the infants were informed about the purpose of the research and gave their written consent. The study was approved by the local Medical Ethics Committee.

Measurements started when infants were about 6 weeks old and continued every four weeks until the age of 26 weeks. Thus, measurement sessions were conducted at 6, 10, 14, 18, 22, and 26 weeks of age. Dates were determined on basis of the corrected age of every infant, that is, ages were calculated from the due date. If the infants were unable to carry out the experimental task due to fussiness or sleepiness, a second ap-pointment was scheduled within 7 days.

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Full-term infants. The mothers of the full-term infants were approached through childbirth education classes, midwives, or gym classes. Their babies were born after a gestation period of 37 to 42 weeks (M = 40.1 weeks; SD = 1.3), had a birth weight above 2800 g (M = 3440 g; SD = 281), and no history of pre- and perinatal complications. All infants of the full-term group scored within their age range on the Bayley Scales of Infant Development (BSID-II; Bayley, 1993) at 12 and 24 weeks of age.

Mean ages at the measurement sessions for the full-term group were 47.7 days, 73.6 days, 103.7 days, 131.1 days, 158.9 days and 188.8 days. Despite attempts to retest after a unsuccessful test date, for 7 infants one test session was missing.

Preterm infants. All preterm infants were admitted to the neonatal intensive care unit (NICU) of the University Hospital Groningen. Clinical data are provided in Table 5.1. The infants’ gestational age ranged from 27.3 to 32.4 weeks (M = 29.6 weeks; SD = 1.8). They had a birth weight between 640 and 2035 g (M = 1267 g; SD = 468). Two of the preterm babies were small for gestational age (SGA, according to Kloosterman, 1970). All preterm infants were screened for retinopathy of prematurity (ROP) around the term age. None suffered of ROP more severe than grade 1. Two infants went through an infection during the neonatal period, indicated by positive blood cultures. To as-sess the possible influence of neonatal illnesses a clinical scoring system was applied at discharge, the Nursery Neurobiologic Risk Score (NBRS; Brazy, Eckerman, Oehler, Goldstein, & O’Rand, 1991). The averaged NBRS of the preterm group was M = 3.3 (SD = 2.0). Two infants had a NBRS of 6, which is associated with an increased risk for de-velopmental problems (Brazy et al., 1991).

Of all preterms brain ultrasound scans were made within the first week after birth and at weekly intervals thereafter until abnormalities had disappeared on two subsequent scans. The scans were interpreted by two radiologists experienced in neo-natal radiology. Five infants had germinal matrix hemorrhages (GMH), four of them grade 1 and one GMH grade 2 (according to Papile, Burstein, Burstein, & Koffler, 1978). In addition, the infant with grade 2 hemorrhage had a venous infarction in the left temporal region. Six infants had periventricular echodensities (PVE) with a duration of more than one week (grade 1 periventricular leukomalacia, PVL, according to de Vries, Eken, & Dubowitz, 1992). The duration of prolonged PVE varied from less than 2 to 5 weeks. None of the infants had cystic periventricular leukomalacia.

Follow-up examinations were performed at the outpatient department at regular intervals. They consisted of a pediatric and a neurological examination. All of the infants developed within the normal range. Two had mild developmental anomalies, especially concerning their motor development. For details of the clinical data of each individual infant (i.e. obstetrical and neonatal variables, findings of the ultrasound scans, outcome), see Table 5.1. Taking into account the developmental outcomes of the preterm infants, the group can be qualified as reasonably homogenous, although the obstetrical and neonatal measures show that the infants have rather diverse clinical histories.

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Tabl

e 5.1.

Clin

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dat

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the

grou

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infa

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27.2

964

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13+

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27

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, PDI

108

2M

29.7

113

25-

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20

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mal

3M

30.7

117

30-

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5-

30

wk

< 1

wk

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gr

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0 m

: nor

mal

4F

28.7

194

5-

4 - 8

5-

60

wk

3 w

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L; P

VL

gr 1

CA 1

9 m

: nor

mal

5M

31.5

718

75-

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3-

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nous

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312

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28.1

497

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mal

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A ge

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l age

; SGA

sm

all f

or g

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PPV

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itiv

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lati

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uppl

em

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ry o

xyge

n re

quir

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t 36

wee

ks p

ostm

enst

rual

age

); N

BRS

Nur

sery

Neu

robi

olog

ic R

isk

Scor

e; P

VE

peri

vent

ricu

lar

echo

dens

itie

s; w

k w

eek/

wee

ks; G

MH

ge

rmin

al m

atri

x he

mor

rhag

e; P

VL

peri

vent

ricu

lar

leuk

omal

acia

; gr

grad

e (a

ccor

ding

to P

apile

, Bur

stei

n, B

urst

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& K

offler

(197

8, G

MH

) and

de

Vri

es, E

ken,

Du

bow

itz

(199

2, P

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); L

left

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ight

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corr

ecte

d ag

e; m

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ths.

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Chapter 5

107


Parents who had indicated their interest in participating in this study together with their baby were contacted after the infants were released from the NICU. For practical reasons, only families who lived up to 50 km away were admitted to the study. They were offered free transportation to the institute and back home. From the group of preterm infants, four infants missed one of the six test sessions. Mean ages at each measurement session were 47.8 days (SD = 5.6), 74.9 days (SD = 6.5), 102.1 days (SD = 5.2), 132.0 days (SD = 6.1), 157.5 days (SD = 3.5), and 183.2 days (SD = 2.6).

ProcedureMeasurement sessions were planned for a time of the day when parents expected

their babies to be alert for 20 to 30 minutes. In the beginning of the test session, infants were given some time to become accustomed to the new environment. When they were in state 3 or 4 of Prechtl’s scale of alertness (awake, eyes open, some spontaneous movements, no crying; Prechtl & Beintema, 1964), the experiment was started.

Infants were presented with a so-called disengagement task. In such a task stimuli can appear at three different positions on a screen: in the center, on the left, or on the right. In this study, the stimuli to the left or right were displayed at 20 degrees eccentricity. The task included two different sorts of trials: competing and non-com-peting trials. All trials started with the appearance of a stimulus in the center of the monitor, the fixation stimulus. The onset of this stimulus was accompanied by a short melody to attract the infant’s attention. After the infant had been fixating the central stimulus for 1 - 2 seconds, the peripheral stimulus was displayed. While in non-com-petition trials the central stimulus disappeared when the peripheral target came up, in competition trials it persisted also after the peripheral target had appeared. After 5 seconds, the stimuli disappeared simultaneously. The screen remained blank for a period of 2.5 seconds, before the following trial began. In Figure 3.1 (see Chapter 3), a schematic representation of the disengagement task is given. Competition trials thus demanded disengagement of attention and gaze from the fixated central stimulus before an eye movement to the peripheral target could be generated. Non-competition trials did not require disengagement, but a simple shift of gaze to the newly appeared stimulus in the periphery. They also serve as control trials for the different stimulus combinations: In a localization task stimuli of about equal physical attractiveness and detectability should not influence the probability or latency of shifting gaze.

ApparatusDuring the tasks the infants were sitting in an infant-seat on a table in a reclined

posture (about 45 degrees) with a light support for their head. In front of the infant-seat a 21 inch monitor was suspended from the ceiling approximately central and perpendicular to the line of gaze. The distance between the monitor and the baby’s eyes was about 35 cm. Only the screen of the monitor was visible. The monitor itself, the equipment necessary to run the tasks and record eye movements, and the experi-

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menter were concealed behind a gray curtain, which filled 180 degrees of the infant’s visual field. The eye movements and the display of the monitor were shown on a SVHS monitor, which allowed the experimenter to run the task on the basis of the babies’ behavior. The infant’s face and eye movements were recorded on video during the experiment. The eye movements were scored off-line from the video recording.

Stimulus Material and Stimulus PresentationTwo different dynamic stimuli were used within the disengagement task: an ab-

stract stimulus and a socially relevant stimulus. The social stimulus consisted of a short video sequence of the face of each infant’s mother. This video recording was made during a first visit of mother and baby to the lab. The mother’s face was recorded while she was smiling and talking with her baby as she normally did. The abstract stimulus was derived from the video of the mother by carrying out several transformations in a graphic computer program (Corel PHOTO-PAINT 9). This procedure ensured that the two stimuli resembled each other regarding their dynamics, color range, etc., but were completely different with respect to their meaning to the infant. Some frames from each type of video are given in the schematic representation of the task (see Figure 3.1, Chapter 3). At the viewing distance of 35 cm, all stimuli subtended a visual angle of 10 by 10 degrees. Thus, the face was much smaller than it would appear to the baby in a normal interaction. As even newborns can recognize a well-known face after a size change (Walton, Armstrong, & Bower, 1997), we expected that the infants would not to have any problems with the size of the face. This was supported by observations during the experiment that infants were very interested in the stimuli and were oc-casionally smiling to the mother stimulus but not to the abstract stimulus.

The experiment contained 32 competition trials and 8 non-competition trials. As reactions to the peripheral stimulus in the non-competition condition were expected to be less variable, fewer non-competition trials were considered to be necessary to provide reliable measurements. Both stimulus types could appear as central stimulus or as peripheral target, which resulted in four different stimulus combinations (face-face, face-abstract, abstract-face, abstract-abstract). These stimulus combinations were presented with equal frequency. Peripheral targets appeared as often on the left as on the right side, and the order in which the trials were presented was randomized. An experimental run normally lasted about 12 minutes. Whenever the infant started fuss-ing or crying or became sleepy, the testing session was interrupted for some time.

AnalysisBehavioral coding. The video recording of the infant’s face was played back half-

frame by half-frame (20 ms intervals) in order to code the eye movements. The direc-tion and the latency of the first eye movement after the appearance of the peripheral stimulus were scored. Also, the frequency of trials when the infant did not move his or her eyes was calculated. Trials in which the infant was not fixating the first stimulus

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when the peripheral stimulus appeared were excluded from the analysis, for example, when the infants had already averted their gaze from the central stimulus or had their eyes closed for various reasons (e.g., blinking, yawning, fussing). Eye movements starting less than 200 ms after the second stimulus appeared, were considered an-ticipatory (Haith, Hazan, & Goodman, 1988) and also dropped from the analyses. All eye movements following the appearance of the peripheral stimulus but not leading to its localization were considered to be errors.

The data were coded by different observers, who had been trained by the first au-thor. Approximately 10% of the sessions were double-coded. Interobserver reliability for the onset of an eye movement was found to be on average 87.2% (range 62.5% to 100%). Cohen’s kappa for the category of first eye movement was on average .87 (range .63 to 1.0).

Statistical analysis. The relative frequency of looks to the peripheral target and the frequency of no eye movement occurring were calculated for each test session and condition. To calculate the latencies of looks, the time differences between the ap-pearance of the peripheral stimulus and the onset of an eye movement to this target were calculated. The median reaction times for each infant, session, and stimulus combination were determined. A plot of all median reaction times revealed that the distribution of the raw data was positively skewed. Therefore a square root transfor-mation of the latency data was executed (Rummel, 1970) before the statistical analyses were carried out. For ease of understanding, the averaged response latencies reported in the text and the reaction times displayed in the figures are given in seconds.

The data were analyzed using a multilevel modeling technique (Snijders & Bosker, 1999; Woodhouse, 1996). Multilevel analysis is a regression procedure for data with a hierarchical structure and complex patterns of variability. When applied to longitudi-nal data, the repeated measures are regarded as “nested” within individuals. Unlike a standard multiple regression model, a multilevel model contains more than one error term: one for every level of the hierarchical data. The model also allows intercept and slope coefficients to vary randomly which means that the association between session scores and explanatory variables may differ between individuals. Another strength of this approach is that it allows for both the number of observations per individual and the spacing of the observations in time to vary.

Multilevel analysis was used to examine whether (a) the frequency and latency of looks and frequency of trials in which the infant did not perform an eye movement changed with age, (b) the combination of stimuli influenced the frequency and latency of looks, and (c) there were differences between the full- and preterm group in the developmental trajectories and in the effects of stimulus combinations. The data of the competition and the non-competition trials were analyzed separately and treated as different subsets of the data. In order to test whether there were differences be-tween the preterm and the full-term group, the variable “prematurity” was added as a 0-1 dummy variable to the models. Also coefficients for the interaction effects were

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included. Furthermore, it was tested whether the residual variance was larger in one of the two infant groups.

All models had three levels: infant, test session, and stimulus combination. Based on earlier research (see e.g., Chapter 3; Butcher et al., 2002), a model of three piecewise linear functions was fit to the data. These studies suggested rapid development for the period from 6 to 9 and from 9 to 16 weeks and a stabilization for the period between 16 and 26 weeks of age. As shifts of gaze to the peripheral target at 6 weeks were very infrequent, reliable latency data were not available for the first measurement point. A model of two piecewise linear functions was therefore used for the reaction time data, with one function from 9 to 16 weeks and another from 16 to 26 weeks. Infants’ test sessions differed in terms of the number of trials carried out as some sessions had to be terminated early due to infants’ fussing or getting sleepy. This was controlled for by adding a correction term to the models. As the infants’ real ages were entered into the model rather than age categories, the variable age could be treated as a con-tinuous variable which provided information on infants’ behavior also between the measurement points.

For the analyses, the data were centered around 12 weeks of age, which was about the middle of the period in which the largest change was expected. Variables for the different age periods and the different stimulus combinations were added to the equation in order to predict the frequency of looks or the reaction times. T tests were implemented to determine the statistical significance of the coefficients. The fit of the model and its improvement was examined using χ2 tests of deviance. T tests were also used as post-hoc tests. Whenever multiple t tests were carried out, Bonferroni corrections were implemented to keep alpha at .05 (Stevens, 1992).

RESULTSFrequency of Shifts of Gaze to the Peripheral Stimulus

The mean group frequencies of looks to the peripheral stimulus in competition and non-competition trials across ages are depicted in Figure 5.1. In the competi-tion condition, the frequency of looks increased gradually from 6.5% (SD = 8.3) at 6 weeks to 61.9% (SD = 22.8) at 14 and 88.0% (SD = 9.1) at 26 weeks of age. However, in the non-competition condition infants shifted their gaze in 57.2% (SD = 31.0) of the trials already at 6 weeks and in 85.9% (SD = 20.8) of the trials at 10 weeks of age. Between 6 and 14 weeks of age, the frequencies of the non-competition condition were signifi-cantly higher than those of the competition condition (6 weeks, t(19) = -7.89, p < .01; 10 weeks, t(29) = -11.27, p < .01; 14 weeks, t(29) = -6.91, p < .01). From 18 weeks on, the gaze shifting frequencies of the competition situation started to approach those of non-competition situations (18 weeks, t(27) = -2.54, p > .10; 22 weeks, t(26) = -3.00, p < .05; 26 weeks, t(28) = .09, p > .10). However, the developmental trajectories of looks to the periphery were highly similar in preterm and full-term infants.

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Figure 5.1. The mean frequency and standard error of looks to the peripheral target in competition and non-competition trials for the preterm (PT) and the full-term (FT) group.

Competition trials. As described earlier, the frequency of gaze shifts to the peripheral target in the competition condition increased throughout the three age periods. The model of the competition trial data correspondingly contained significant age coef-ficients for the age period of 6 to 9 weeks (t(163) = 2.57, p < .05), 9 to 16 weeks (t(163) = 11.64, p < .001), and 16 to 26 weeks (t(163) = 5.23, p < .001). However, the coefficient of age for 9 to 16 week function was significantly larger than the one of the 16 to 26 week function (slope coefficients β9-16 = 1.09 versus β16-26 = .28.), which indicates a more gradual increase in shifts of gaze after 16 weeks of age. This was confirmed by the significant gain in fit which was obtained when using separate age coefficients for the periods of 9 to 16 and 16 to 26 weeks compared to only one age coefficient for the period of 9 to 26 weeks (χ2(1) = 38.20, p < .001). Consistent with this, post-hoc comparisons of mean group frequencies of looks in consecutive sessions were still significant between 18 and 22 weeks (t(24)= -3.87, p < .01), whereas between 22 and 26 weeks of age there was no significant increase demonstrable anymore (t(26) = -.88, p > .10).

In Figure 5.2, the development of the frequency of looks to the peripheral target is depicted for the different stimulus combinations. The effect of the different stimulus combinations was tested by adding three of the four possible combinations as a 0-1 dummy variable to the model and contrasting them against the fourth category, the combination face-face. There were two significant main effects of stimulus combina-tion: When controlling for age, the combination face-abstract elicited significantly more shifts of gaze to the peripheral stimulus than the reference combination face-face (t(648) = 6.15, p < .001), whereas under the condition abstract-face less gaze shifts were observed (t(648) = -4.24, p < .001). No significant difference was found between

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the stimulus combinations face-face and abstract-abstract.

Figure 5.2. The mean frequency and standard error of looks in competition trials per stimulus combina-tion between 6 and 26 weeks of age.

There were three significant interactions between stimulus combination and age period: During the age period of 6 to 9 weeks, the increase in gaze shifting frequency was significantly smaller for the stimulus combination abstract-face (t(648) = -2.69, p < .01) and greater for the combination face-abstract (t(648) = 2.43, p < .05) than it was for the reference combination face-face. While the frequency of looks in the stimulus combination face-abstract increased from 7.5% (SD = 18.4) to 46.2% (SD = 27.6) between 6 and 10 weeks, in the abstract-face combination it grew from 11.0% (SD = 16.8) to only 20.8% (SD = 18.8) in the same period of time. The third interaction, the interaction of the stimulus combination face-abstract with the age period of 16 to 26 weeks (t(648) = -3.90, p < .001) implies that in the last age period the frequency of looks changed less when the central stimulus was a face and the peripheral stimulus was abstract than in the face-face condition. As can also be seen in Figure 5.2, the frequency of gaze shifts in the face-abstract condition had almost already reached its maximum by 18 weeks (18 weeks, M = 82.2%, SD = 5.0; 22 weeks, M = 86.2%, SD = 3.5; 26 weeks, M = 92.0%, SD = 2.7), which resulted in the smaller increase throughout the 16 to 26 weeks age period.

The analysis of random effects revealed that the residual variance depended on whether the infant belonged to the preterm or full-term group (χ2(1) = 5.10, p < .05). The effect was caused by a larger variance in performance of preterm compared to the full-

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term infants. Further, a significant estimate of intercept variance (χ2(1) = 16.88, p < .001) was found. This indicates that the frequency of gaze shifts differed significantly between infants at 12 weeks of age. Further, there were significant differences between infants between 16 and 26 weeks concerning the slope of the function (χ2(1) = 6.18, p < .05).

Figure 5.3. The mean frequency and standard error of looks in competition trials per stimulus combina-tion for (A) the preterm and (B) the full-term group.

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Figure 5.3 shows the developmental trajectories for the different stimulus combi-nations for both (A) the preterm and (B) the full-term group. The common model of the preterm and full-term infants yielded no significant differences between the two groups, and there were no significant interaction effects involving the variable pre-maturity, either. This indicates similar developmental trajectories in both groups.

However, although the group of full-term infants and the group of preterm infants did not differ concerning their frequency of looks to a peripheral target, there are some results which suggest that disengagement of attention was less efficient in the preterm group. The frequency of the lack of an eye movement in reaction to the newly appeared peripheral stimulus in pre- and full-term infants is displayed in Figure 5.4. While 6-week-old preterm infants did not shift their gaze away from the central stimulus in 86.7% (SD = 32.4) of the trials, full-term infants of the same age kept on staring to it in only 61.3% (SD = 8.8). The multilevel model predicting the frequency of trials in which the infant did not perform an eye movement correspondingly contained a significant interaction of the first age period and the variable prematurity (t(162) = -2.11, p < .05). A t test for independent samples as post-hoc test also revealed a significant difference in the frequency of staring at 6 weeks of age (t(19.26) = -2.87, p < .05).

Figure 5.4. The mean frequency and standard error of staring in competition and non-competition trials for the preterm (PT) and the full-term (FT) group.

Non-competition trials. As can be seen in Figure 5.1, the overall percentage of shifts of gaze to the peripheral target in non-competition trials increased significantly be-tween the first measurement session at 6 and the second measurement session at 10

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weeks of age. No significant changes in gaze shifting frequency occurred after the age of ten weeks. This was indicated by the variable age having a significant coefficient for the 6 to 9 week function (t(162) = 4.45, p < .001), but not for the 9 to 16 week function and the 16 to 26 week function.

Figure 5.5. The mean frequency and standard error of looks in non-competition trials per stimulus combination for (A) the preterm and (B) the full-term group.

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Infants differed in the rate at which gaze shifts increased between 6 and 9 weeks of age as the significant slope variance for the 6 to 9 week function (χ2(1) = 7.63, p < .01) indicates.

However, there was no effect of stimulus combination on the frequency of looks. The frequency of gaze shifts in the non-competition trials did not depend on whether an infant was born prematurely or not, either. This can be seen in Figure 5.5, which depicts the development of gaze shifts to the peripheral target for both (A) the preterm and (B) the full-term group.

Like in the competition condition, there were also in this simple gaze shifting task indications that preterm infants were performing less efficiently than full-term infants during the first measurement session. As Figure 5.4 shows, at 6 weeks of age, the pre-term infants kept on staring to the center of the monitor even after the stimulus was gone and the peripheral target had appeared in 15% (SD = 9.57) of the trials, whereas the full-term infants did so only in 9.53% (SD = 7.53) of the trials. This occurred mainly when the young preterm infants were supposed to look from the mother stimulus to the abstract one (t(595) = -4.08, p < .001) or the other way around (t(595) = -2.52, p < .05).

Figure 5.6. The mean latency and standard error of looks to the peripheral target in competition and non-competition trials for the preterm (PT) and the full-term (FT) group.

Latency of Shifts of GazeThe median latency of looks to the peripheral target in the competition and

non-competition situation for both infant groups is displayed in Figure 5.6. The first

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measurement point was excluded from the analysis, as it was based on only very few data points.

As can also be seen from Figure 5.6, infants shifted their gaze faster in non-com-petition trials than in competition trials. Although the median reaction times of the competition and non-competition condition were converging throughout the testing period, they were significantly different at young ages (10 weeks, t(25) = 5.46, p < .01; 14 weeks, t(26) = 4.67, p < .01) as well as at the later measurement points (18 weeks, t(26) = 6.87, p < .01; 22 weeks, t(26) = 4.11, p < .01; 26 weeks, t(28) = 2.99, p < .05).

Competition trials. The median reaction time of both preterm and full-term infants dropped throughout the entire testing period. While it took infants of 10 weeks on average more than a second to shift their gaze, this time decreased throughout the measurement period to about 500 ms. The coefficient of the variable age was significant for the age period of 9 to 16 (t(136) = -5.41, p < .001) and 16 to 26 weeks (t(136) = -3.49, p < .001). The two age coefficients (β9-16 = -.0072, β16-26 = -.0022) differed significantly from each other (χ2(1) = 14.26, p < .001), suggesting a less rapid decline during the last age period.

The multilevel analysis revealed a significant effect of group (t(28) = -2.52, p < .05) with the preterm infants exhibiting shorter latencies than the full-term infants when controlling for age. In the age period between 16 and 26 weeks, the interaction of the variables prematurity and age was significant (t(136) = 2.43, p < .05), indicating that the effect of preterm infants exhibiting shorter latencies disappeared as infants grew older. However, when three-way interactions were added to the model, the interaction of prematurity, the stimulus combination abstract-abstract, and the age period from 16 to 26 weeks yielded a significant effect (t(524) = 2.30, p < .05), while the two-way interaction between the variables age and prematurity remained a trend (t(136) = 1.91, p < .10). In Figure 5.7 the change in median reaction times of the full-term and the preterm group is depicted for the four different stimulus combinations. In all stimulus combination conditions the preterm infants showed faster gaze shifts than their full-term age mates during the first few months of the measurement period, but after 16 weeks this effect diminished. This was particularly the case for the stimulus combination abstract-abstract: Here, the gaze shifting latency in preterm infants from the age of 16 weeks on age tended to be even larger than in full-term infants of the same age.

The multilevel analysis also revealed a main effect of the stimulus combination abstract-face (t(525) = 3.41, p < .001). It indicates that – when controlling for age and prematurity – infants were slower in shifting their gaze away from an abstract stimulus to a face in the periphery compared to the reference condition face-face.

The estimate of slope variance was significant for the 9 to 16 (χ2(1) = 7.05, p < .01) and the 16 to 26 weeks period (χ2(1) = 3.22, p < .10). Infants thus differed considerably concerning the rate at which their gaze shifting latency decreased. Again, the residual variance depended on whether the infant belonged to the preterm or full-term group

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(χ2(1) = 19.48, p < .001). However, in this case preterm infants showed a smaller variance in performance than the full-terms.

Figure 5.7. The mean latency and standard error of looks to the peripheral target per stimulus combination in competition trials for the preterm (PT) and the full-term (FT) group.

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Non-competition trials. As can be seen in Figure 5.6, also in the non-competition situation the median reaction time decreased significantly throughout the measure-ment period. The age coefficients of the 9 to 16 (t(154) = 4.18, p < .001) and the 16 to 26 weeks period (t(154) = 4.73, p < .001) yielded significance. However, post-hoc t tests revealed that the gaze shifting latency decreased between 14 and 18 weeks of age (t(26) = 4.22, p < .01), but not between 18 and 22 (t(23) = -1.16, p > .10) and 22 and 26 weeks (t(25) = -1.52, p > .10) of age anymore. This indicates that the decrease in median reaction time came to an end as infants grew older. There were no main effects of stimulus combination or group effect and no interaction effects, either. In the analysis of the random effects, the estimate of the intercept variance was significant (χ2(1) = 5.59, p < .05).

DISCUSSIONThe Development of Simple Shifts of Gaze and Disengagement

The overall developmental changes of attention and gaze shifting are – taken by and large – in accord with earlier results. While infants shifted their gaze effectively in the non-competition condition already from 10 weeks on (see e.g., Butcher et al., 2000), the persistence of a central stimulus as in the competition condition lowered the probability of looks to the peripheral stimulus in younger infants (see e.g., Aslin & Salapatek, 1975; Harris & MacFarlane, 1974). At 18 and 26 weeks of age, there were no differences in gaze shifting frequency anymore between the competition and the non-competition condition. The latency of gaze shifts decreased throughout the measure-ment period in both conditions. Saccadic reaction times in situations with competing stimuli were longer than in non-competing situations both in infants younger than 3 months as demonstrated also by Matsuzawa and Shimojo (1997) and in older infants as shown before by Hood and Atkinson (1993).

Differences in Gaze Shifting Behavior between Preterm and Full-term InfantsIt was the goal of this study to examine differences in gaze shifting behavior

between the preterm and the full-term group under different conditions: in situa-tions with competing and non-competing stimuli and with different combinations of stimuli.

Simple gaze shifting (without disengagement). Concerning simple shifts of gaze, there were few differences found between the full-term and the preterm group. Both groups showed about the same frequencies of looks to the periphery in the non-competition condition throughout the measurement period. The latencies of gaze shifts and their developmental trajectory were not significantly different for full- and preterms, either. However, at 6 weeks of age preterm infants kept on looking to the center of the display more often, even after the stimulus had disappeared and a peripheral one had come up. Although this effect was relatively small and occurred only in the face-abstract and the abstract-face condition, it suggests that young preterm infants were performing

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somewhat less efficiently than their full-term age mates. These results are in accord with studies which report gaze shifting problems in preterms, although mostly in the form of longer latencies (Masi & Scott, 1983; Landry et al., 1985; Friedman et al., 1981; Vervloed, 1995). However, the small disadvantage of the preterms was only temporary, and for the most part their performance and developmental trajectories were similar to full-term infants.

Shifts of gaze which require disengagement of attention. When infants had to disengage their attention before shifting their gaze to the peripheral stimulus, there were again no differences between full- and preterm infants concerning the frequency of gaze shifts and its development. But the young preterm infants had clearly more problems with sticky fixation than their full-term age mates: At 6 weeks, preterm infants tended to keep on looking to the central stimulus more often than their full-term age-mates did. This effect had disappeared by 10 weeks of age. In contrast, the preterm infants also showed an advantage in latency when they shifted their gaze to the periphery. They were faster in disengaging and shifting their gaze until about 16 weeks of age. Thus when young preterm infants overcame sticky fixation, which they did less fre-quently than their full-term age-mates, they tended to shift their gaze more quickly to the peripheral stimulus.

Variance in performance. The variance in task performance was different for the preterm and the full-term group. In the preterm group, the variance in performance concerning the frequency of disengagement was larger, while it was smaller for the latency of disengagement. As a larger variance can also be indicative of a worse per-formance, these findings fit with the rest of results: Preterm infants had difficulty in overcoming staring behavior, but performed more efficiently in generating eye movements.

The analyses also revealed significant differences in the frequency and latency of gaze shifting and especially in the rate at which these parameters developed between infants which is in accord with earlier findings (Butcher et al., 2000). Large inter-individual differences tended to occur during periods of rapid change.

Effects of Stimulus CombinationIn this study, different combinations of stimuli were used to examine the effect of

socially relevant and abstract stimuli on gaze and attention shifting. We have described in another study how healthy full-term infants reacted to a gaze shifting task with different stimulus combinations (see Chapter 3). Preterm infants have been reported to react differently to faces (Field, 1977, 1979; Masi & Scott 1982; Barratt et al., 1992) and unknown stimuli (Sigman, 1983; Rose et al., 1979) compared to full-term infants. However, in this study, a remarkable consistency of preterm infants’ reactions to the different stimulus combinations with the full-term infants was found:

No effects of stimulus combination were found in the non-competition condition concerning frequencies or latencies of gaze shifts. This was in agreement with the

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expectations, as in a task which only requires simple gaze shifts stimuli of compa-rable physical salience should not elicit differences in the frequency and latency of stimulus localization. However, in the competition condition infants disengaged their gaze more frequently when the central stimulus was a face and the peripheral stimu-lus was abstract and less frequently and also more slowly in the opposite condition (abstract-face). The interaction effect of the factors age and stimulus indicated that these differences were most pronounced when the ability to disengage gaze and at-tention was developing, but not yet well established. At 6 weeks of age, infants kept on looking to the central stimulus once they fixated it, regardless of what was ap-pearing in the periphery. From 22 weeks on, they shifted their gaze reliably between all four stimulus combinations. The frequency of looks for the stimulus combination face-abstract increased most rapidly and reached its final level already at 18 weeks, while for the stimulus combination abstract-face full capacity of disengagement was reached approximately 4 weeks later. Both stimuli – the central fixation stimulus and the peripheral target – influenced the frequency of looks to the periphery, which is concordant with results described by Finlay and Ivinskis (1984). The – by this time well-known (Barrera & Maurer, 1981) – infant’s mother’s face was less attractive than the relatively new, salient abstract stimulus for the preterm as well as the full-term group. However, while preterm infants in general tended to shift their gaze between two competing stimuli as fast or even faster than full-term infants, from 16 weeks of age on, they seemed to have some difficulties in looking away from an abstract stimu-lus. This can be interpreted as a sign of slower habituation to a new stimulus, which has been reported earlier in preterm infants (e.g., Sigman et al., 1986).

Extra Visual Input and Attentional DevelopmentWe know of two earlier studies which examined the development of simple gaze

shifts and disengagement in pre- and full-term infants (Butcher et al., 2002; Atkinson, 2000). They found shorter latencies of preterm infants’ gaze shifting in competition and non-competition situations and interpreted this effect as a benefit of experience in sensory-motor processing. Following their account, later developing skills, such as disengagement, should not benefit from extra visual input. But the results of this study suggest that the changes in the development of attention due to a preterm birth and early visual experience are not so clear-cut. While preterm and full-term infants did not differ concerning the latency of simple gaze shifts, additional visual input was associated with a short-lasting facilitation of the execution of shifts of gaze from fixation. However, in this study preterm infants were also shown to have more difficulty in overcoming staring behavior. This finding suggests that the triggering of a gaze shift and its execution are not indissolubly associated, but might be two rather independent processes.

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ConclusionAs described above, there have been differences in opinion on whether early visual

input is beneficial for an infant or whether it might be detrimental to the developing visual system. The results of this study do not support one of the two accounts, but suggest that extra visual experience changes the visual and attentional development of an infant in general with positive effects on the one hand and a negative impact on the other. However, the effects were shown to be temporary – by the end of the measurement period there were no relevant differences in attention and gaze shifting performance detectable anymore between the two groups of infants.

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Yarrow, L. J., Klein, R. P., Lomonaco, S., Morgan, G. A. (1975). Cognitive and motivational development in early childhood. In B. Z. Friedlander, G. M. Sterritt, & G. E. Kirk (Eds.), Exceptional infant (Vol. 3, pp. 491-503). New York: Brunner-Mazel.

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Chapter 5

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University of Groningen Through the Eyes of an Infant …Infant attention patterns have been reported to be related to later intellectual functioning (see e.g., Colombo, 1993; Yarrow,