توانایی هجده ماهه، برای پیش بینی نگاه بدنبال حواس پرتی و یا یک تاخیر طولانی

Abstract The abilities to flexibly allocate attention, select between conflicting stimuli, and make anticipatory gaze movements are important for young children's exploration and learning about their environment. These abilities constitute voluntary control of attention and show marked improvements in the second year of a child's life. Here we investigate the effects of visual distraction and delay on 18-month-olds’ ability to predict the location of an occluded target in an experiment that requires switching of attention, and compare their performance to that of adults. Our results demonstrate that by 18 months of age children can readily overcome a previously learned response, even under a condition that involves visual distraction, but have difficulties with correctly updating their prediction when presented with a longer time delay. Further, the experiment shows that, overall, the 18-month-olds’ allocation of visual attention is similar to that of adults, the primary difference being that adults demonstrate a superior ability to maintain attention on task and update their predictions over a longer time period.

. Introduction In the first years of life, the development of attentional control provides an important mechanism for children's exploration and learning about their environment. Attentional control involves the ability to flexibly allocate attention and suppress conflicting stimuli that interfere with the task at hand. The early development of this ability has been suggested to underpin the development of more complex skills, such as emotional and social regulation (Posner, Rothbart, Sheese, & Voelker, 2012) executive functions (e.g., working memory and inhibition; see Garon, Bryson, & Smith, 2008 for a review), and language development (Salley, Panneton, & Colombo, 2012). Further, deficits in the early development of attentional control may be related to increased risk for developmental disorders (e.g., attention deficit hyperactivity disorder and autism spectrum disorder) (Johnson, 2012). It is generally believed that brain maturation and increased functional connectivity are accompanying developmental improvements in behavioral control of attention. Resting-state fMRI studies indicate that the neural networks, supporting basic forms of attention control, become functional in infancy. They show a strong increase in connectivity over the first 2 years of life, and follow different developmental trajectories (Gao et al., 2013, Gao et al., 2009 and Uddin et al., 2010). Functional connectivity between brain areas that support resolution of attentional conflict, such as the suppression of interfering stimuli (e.g., connectivity between the frontal cortex and anterior cingulate gyrus), emerges after 6 months of age and has a protracted development that lasts throughout childhood (Petersen and Posner, 2012 and Posner and Fan, 2008). One method to study attentional control in infancy and toddlerhood is the assessment of anticipatory gaze, that is, gaze shifts occurring prior to the presentation of an event or stimulus. Studies measuring eye movements have shown that infants can make anticipatory gaze shifts around 4–9 months of age (Johnson et al., 1991, Nelson, 1971 and Sheese et al., 2008), depending on the difficulty of the task. In contrast to reactive gaze shifts, anticipatory eye movements are generally thought to rely on voluntary attentional processes and to be an early marker of attentional control. By the end of the first year infants demonstrate improvements in their ability to resolve visual attentional conflict as seen in their enhanced performance on tasks that involve switching gaze response, such as in looking versions of the A-not-B task (e.g., Cuevas and Bell, 2010 and Watanabe et al., 2012). The A-not-B task requires the ability to cope with conflicting mental representations (i.e., previous hiding location vs. current hiding location) and the suppression of a previously learned response in favor of an updated prediction. Thus, successful performance includes flexibly shifting direction of attention when the target's hiding location is switched from location A to location B, which in turn has been associated with increased activation in the frontal and parietal areas in infancy (Baird et al., 2002 and Cuevas and Bell, 2011). Studies using manual search versions of the A-not-B task have shown that by the end of the first year and throughout toddlerhood, children are increasingly able to deal with longer delays between hiding and searching (Marcovitch & Zelazo, 1999), or increasing conflict (Schutte, Spencer, & Schöner, 2003), but they can still be found to make search errors on this task at pre-school age (Espy, Kaufmann, McDiarmid, & Glisky, 1999). In a recent study (Watanabe et al., 2012), we used a looking version of the A-not-B task to assess 10- and 12-month-old infants’ ability to correctly anticipate the reappearance of a hidden target during both pre- (A) and post-switch (B) trials. By using eye-tracking we were able to measure the infants’ visual attention to both the correct and incorrect location quantitatively throughout the task. The study showed that an age-related improvement in attentional control takes place between 10 and 12 months of age. This age-related improvement was particularly reflected in less perseverative anticipatory looking (i.e., less anticipatory looking at the incorrect hiding location on the B trials) in the older age group. In one condition the infants were presented with a visual distractor that preceded the reappearance of the target on the B trials and thereby increased the level of attentional conflict of the task. The infants in the visual distractor condition showed more perseverative anticipatory looking compared to the infants in the control condition where no visual distractor was presented. The result also indicated that the 12-month-olds were better than the 10-month-olds at handling the distractor, but also that older infants’ ability to overcome distraction was not yet sufficiently developed. This finding suggests that attentional control and the ability to overcome attentional conflict is still under development by the end of the first year. Thus, to further our understanding of this development it would be fruitful to further examine the developmental course of this ability. Current research suggests that marked improvements in the ability to control attention take place between 18 and 24 months of age (Clohessy et al., 2001, Garon et al., 2008 and Posner et al., 2012). In line with Colombo's (2001) view, that research on cognitive development gains from focusing on age periods where rapid improvements take place, in the present study we focus on 18-month-old children's ability to control attention and we contrast our results to that from adults and from our previous study on infants. For the current study we adapted our previously used looking version of the A-not-B task (Watanabe et al., 2012), which included a control and visual distractor condition. Eighteen-month-old children's and adult's anticipatory looking, on four A (pre-switch) and two B (post-switch) trials, was examined following a 3.5 s hiding delay. The A trials were identical, whereas a visually distracting stimulus was added in the visual distractor condition on the B trials. In addition, we included a long delay condition where the duration of the target's hiding delay was extended to 10 s on the B trials. The purpose of adding a longer delay was to assess how the increased time needed to keep information in mind (i.e., the target's correct hiding location) would affect the participants’ allocation of anticipatory looking. We presumed that this condition would be more challenging for the participants in terms of working memory demand compared to the control condition. Working memory is an ability that is closely linked to attentional control and these two cognitive processes rely on overlapping brain regions (e.g., parietal and prefrontal cortex) (Corbetta and Shulman, 2002 and McNab and Klingberg, 2008). Whereas attentional control is important for selecting between and suppressing conflicting information, working memory is necessary for actively maintaining and retaining information (Kastner et al., 2007). To our knowledge, no previous study has examined how both distraction and an increase in time delay affect 18-month-olds’ ability to make correct anticipatory gaze predictions on a task that requires the ability to control visual attention. Considering our previous findings from 10- to 12-month-olds (Watanabe et al., 2012), we expected the 18-month-olds to correctly anticipate the target's location on the A trials and also on the B trials in the control condition (i.e., a 3.5 s empty hiding interval). In the same study Watanabe et al. (2012) found that the introduction of a distractor deteriorated anticipatory looking performance in 10–12-month-olds. We used the same distractor in the present study to investigate whether the ability to suppress this conflict has matured by 18 months of age. In the long delay condition, we predicted the 18-month-olds to display less accurate anticipatory looking on B trials compared to the children in the control condition. This could be revealed in both more perseverative anticipatory looking and/or less correct anticipatory looking. Finally, given the central role of the maturation of the attentional control system for the current task we expected that the adults would outperform the 18-month-olds across trials (A and B) and conditions. By comparing how the allocation of attention is managed for adults and for children at the age when they presumably are starting to master the task we hope to improve our understanding of the development of attentional control.

3. Results Following the approach of our previous study (Watanabe et al., 2012) we analyzed absolute looking times to the correct and incorrect occluders during the time windows of interest. Descriptive data of mean anticipatory looking time at the correct and incorrect occluder during 2 s (i.e., a time window following the sound cue and before the target's reappearance) on the A and B trials and during 9 s (the extended time period) on the first B trial are presented in Table 1 for each condition and age group. For descriptive purposes mean looking times to the central area (i.e., an aligned area between the two occluders) and looking times elsewhere (i.e., looking times elsewhere on the display and/or outside the display) are also presented in Table 1. In the analyses that follow we examine 18-month-olds’ anticipatory looking before and after the switch of hiding location in the three conditions and compare these effects to those observed in adults. Table 1. Mean anticipatory looking time (s) at the correct and incorrect occluder, c-area (central area located between the correct and incorrect occluder), and elsewhere (on the display or outside the display) during 2 s (following the sound cue) on the A and B trials and during the extended time period (9 s divided into 3 time intervals: 0-3 s, 3-6 s, and 6-9 s, following the sound cue) on the first B trial in each condition and age group. 18-month-olds Adults Control condition Distractor condition Long delay condition Control condition Distractor condition Long delay condition M SD M SD M SD M SD M SD M SD A trials Correct .90 .37 .96 .58 .82 .35 1.34 .55 1.64 .32 1.32 .55 Incorrect .27 .27 .22 .20 .22 .22 .20 .25 .14 .22 .14 .20 C-area .13 .13 .14 .20 .15 .13 .13 .19 .04 .05 .19 .43 Elsewhere .68 .50 .63 .47 .81 .40 .32 .47 .17 .22 .35 .37 B trials Correct .72 .54 .66 .49 .36 .44 1.51 .62 1.14 .50 1.51 .58 Incorrect .24 .22 .31 .43 .27 .37 .11 .12 .09 .21 .03 .08 C-area .08 .11 .39 .40 .12 .22 .25 .53 .56 .46 .15 .37 Elsewhere .94 .52 .64 .59 1.26 .53 .13 .28 .21 .21 .31 .34 1st B trial (0-3 s) Correct 1.21 .96 1.05 .93 .77 .82 2.27 .83 1.72 .86 2.36 .72 Incorrect .49 .52 .51 .79 .66 .90 .35 .55 .15 .31 .07 .16 C-area .14 .24 .43 .67 .16 .28 .21 .53 .73 .86 .28 .58 Elsewhere 1.10 .91 1.01 .99 1.46 .99 .17 .62 .40 .48 .30 .41 1st B trial (3-6 s) Correct .92 .91 .92 .82 .42 .57 2.49 .47 1.90 .94 2.00 .93 Incorrect .43 .58 .29 .57 .47 .48 .27 .35 .21 .28 .20 .39 C-area .13 .25 .30 .39 .26 .40 .09 .17 .57 .86 .26 .62 Elsewhere 1.46 1.00 1.51 .99 1.85 .87 .15 .30 .32 .46 .54 .68 1st B trial (6-9 s) Correct .59 .66 .48 .73 .53 .54 2.32 .52 2.03 .84 1.97 .90 Incorrect .38 .55 .17 .28 .41 .41 .40 .50 .32 .45 .24 .58 C-area .10 .17 .22 .44 .17 .32 .13 .17 .32 .62 .33 .71 Elsewhere 1.91 .94 2.14 .87 1.89 .93 .16 .33 .33 .42 .46 .55 Table options 3.1. Anticipatory looking on A trials For illustrative purposes, Fig. 2 shows the 18-month-olds’ and adults’ mean looking time at the correct and incorrect occluders continuously during the A trials (averaged across the four trials). An inspection of the figure suggests that the adults tend to keep their gaze at the correct occluder (A), whereas the children show a more distinct decrease in looking at occluder A following the target's disappearance. A general decrease in looking at the AOIs (occluder A and B) means that the participant looked somewhere else on the screen or outside the screen. Relevant findings related to anticipatory looking time at the two occluders and age effects are presented in the analyses below. An illustration of mean looking in seconds averaged across the four A trials for ... Fig. 2. An illustration of mean looking in seconds averaged across the four A trials for the 18-month-olds (left) and the adults (right) throughout the whole trials. The solid and dotted lines represent looking time at the correct (A) and incorrect (B) occluders, respectively. Error bars represent ±standard error. Figure options Mean looking time during the 2 s interval after the sound cue and before the reappearance of the target, averaged over the four A trials, was analyzed in a 3 × 2 × 2 mixed repeated measures analysis of variance (ANOVA) with condition (between factors; control vs. visual distractor vs. long delay; the assigned conditions during the B trials that followed), area (within factors; A vs. B), and age group (between factors; 18-month-olds vs. adults) as independent variables. The ANOVA showed that the main effects of area, F(1, 91) = 246.85, p = .000, partial η2 = .73, and age group, F(1, 91) = 25.96, p = .000, partial η2 = .22, were significant. The participants looked more at the correct occluder (M = 1.10 s) than the incorrect occluder (M = .21 s) and the adults (M = 1.60 s) had higher total looking time than the children (M = 1.14 s). The ANOVA also revealed a significant interaction between area and age group, F(1, 91) = 25.12, p = .000, partial η2 = .22, all other Fs < 2.14 and ps > .123. Planned follow-up analyses demonstrated that the adults had more anticipatory looking at the correct occluder than the children, t(95) = 5.53, p = .000, Madults = 1.44 s, M18-month-olds = .90 s, but there was no significant difference in looking at the incorrect occluder, t(95) = 1.65, p = .102, Madults = .16 s, M18-month-olds = .24 s. These results show that the participants in both age groups correctly anticipated the target's reappearance and that the adults’ higher total looking time was reflected in more looking at the correct occluder. 3.2. Anticipatory looking on B trials We next conducted the same analysis on the B trials to clarify whether the children would correctly anticipate the target's reappearance following the switch of hiding location and also to examine possible effects of conditions and age. As no significant interaction was found between trial (First B trial vs. Second B trial) and condition, or trial and area, in either age group (ps > .20), we examined mean anticipatory looking time during a 2 s interval immediately after the sound cue, averaged over the two B trials. The results of the ANOVA revealed significant main effects of area, F(1, 91) = 130.41, p = .000, partial η2 = .59, and age group, F(1, 91) = 31.92, p = .000, partial η2 = .26. The participants had more anticipatory looking at the correct occluder (B) compared to the incorrect occluder (A) and the adults displayed higher total looking time compared to the children, see Fig. 3. 18-month-olds’ (left) and adults’ (right) mean anticipatory looking time (s) ... Fig. 3. 18-month-olds’ (left) and adults’ (right) mean anticipatory looking time (s) during 2 s after the sound cue in the B trials. The solid and dotted lines represent looking time at the correct (B) and incorrect (A) occluders, respectively. Error bars represent ±standard error. Figure options These main effects were modified by significant interactions between area and age group, F(1, 91) = 49.71, p = .000, partial η2 = .35 and a borderline significant interaction between condition and age group, F(2, 91) = 3.06, p = .052, partial η2 = .06, all other Fs < 2.05 and ps > .134. Planned follow-up analysis of the effect of age group on anticipatory looking, using one-way ANOVAs, demonstrated that the adults displayed more correct anticipatory looking, F(95) = 50.00, p = .000, and less incorrect anticipatory looking, F(95) = 10.33, p = .002, than the 18-month-olds. To further understand the interaction effects and to test our a priori hypotheses of effects of condition on the 18-month-olds’ anticipatory looking, we conducted planned comparisons of looking time at the incorrect and correct occluder separately for the age groups. One-way ANOVAs revealed no significant effects of condition on anticipatory looking in the adult age group, whereas a borderline significant effect of condition on anticipatory looking at the correct occluder was found for the 18-month-old age group, F(2, 58) = 3.08, p = .054, all other Fs < 1.68, ps > .20. As indicated by Fig. 3 the children displayed less correct looking in the long delay condition compared with the other two conditions. Pairwise comparisons revealed a significant difference for the comparison of the long delay with the control condition (p = .023) and borderline significant difference for the comparison of the long delay with the distractor condition (p = .058), all other ps > .516. These results show that the adults’ anticipatory looking was similar irrespective of condition, whereas the 18-month-olds showed less anticipatory looking at the correct occluder in the long delay condition compared to the control condition. As supplemental information, to clarify age-related improvements in 18-month-old children's ability to suppress conflicting distraction, we analyzed data on 10-, 12- (from our previous study; Watanabe et al., 2012), and 18-month-old's anticipatory looking to the correct and incorrect location in the distractor condition on B trials. These results suggest that age-related improvements in the ability to control attention take place between 10 and 18-months of age (see supplemental information and SI Fig. 1). 3.3. Anticipatory looking during the extended time period in the first B trial To allow for an examination of how anticipatory looking is maintained over time, the time period between the presentation of the sound cue and the target's reappearance was extended to 9 s in the first B trial. We examined looking time to the correct and incorrect area and also possible effects of conditions, age group, and time interval. The ANOVA revealed significant main effects for area, F(1, 91) = 38.16, p = .000, partial η2 = .30, and age group, F(1, 91) = 69.14, p = .000, partial η2 = .43, and a borderline significant main effect for condition, F(2, 91) = 3.09, p = .050, partial η2 = .06. The significant main effects indicated higher total looking time at the correct occluder compared to the incorrect occluder and also that the adults had overall higher total looking time compared to the 18-month-olds across the 9 s extended period (see Fig. 4). The borderline significant main effect of condition reflected a tendency to overall more looking time in the control condition compared to the other two conditions (Mcontrol = 5.50 s; Mdistractor = 4.48 s; Mlongdelay = 4.61 s). 18-month-olds’ (left) and adults’ (right) mean anticipatory looking time (s) at ... Fig. 4. 18-month-olds’ (left) and adults’ (right) mean anticipatory looking time (s) at the correct (solid line) and incorrect (dotted line) occluder in the three conditions during the extended time period (9 s, divided into three time intervals: 0–3 s, 3–6 s, and 6–9 s) in the first B trial following the presentation of the sound cue. Error bars represent ±standard error. Figure options The ANOVA also showed significant interactions between area and age group, F(1, 91) = 74.05, p = .000, partial η2 = .45, area and time interval, F(2, 91) = 135.78, p = .000, partial η2 = .60, and area, time interval and age group, F(1, 91) = 53.82, p = .000, partial η2 = .37, all other Fs > 2.15 and ps < .076. To clarify these interactions and to further understand the ability of the 18-month-olds’ ability to maintain anticipatory looking during the extended time interval pairwise comparisons of looking time to the correct and incorrect occluder in the three conditions and the three time intervals were performed. The 18-month-olds in the control condition looked more to the correct occluder during the first two time intervals (0–3 s: p = .017; 3–6 s: p = .061; 6–9 s: p = .247); in the distractor condition they looked more to the correct occluder in the second time interval (0–3 s: p = .110; 3–6 s: p = .021; 6–9 s: p = .091); and in the long delay condition they looked equally to the correct and incorrect occluder in all three time intervals (0–3 s: p = .839; 3–6 s: p = .825; 6–9 s: p = .264). These findings are illustrated in Fig. 5, where it can first be seen that in all three conditions the 18-month-olds’ looking time to the correct occluder decreases after the target's disappearance. In the control and distractor condition the children display a relative increase in looking time at the correct occluder following the presentation of the sound cue. This increase in looking time at the correct occluder is most pronounced (but slightly delayed) in the distractor condition and can be explained by the fact that the children's gaze is drawn to the center of the screen during the presentation of the visual distractor, whereas the children in the control condition to a greater extent maintain their gaze at the correct occluder. The children in the long delay condition, on the other hand, show a more distinct increase in looking time at the incorrect occluder compared to the correct occluder following the sound cue, although the amount of looking time at the two occluders is relatively equal. Illustrates 18-month-olds’ mean looking time in the first B trial across the ... Fig. 5. Illustrates 18-month-olds’ mean looking time in the first B trial across the first 22 s in the control (left) and distractor (middle) conditions, and across 28 s in the long delay (right) condition. The solid and dotted lines represent looking time at the correct occluder (B) and incorrect occluder (A), respectively. In the control and visual distractor conditions, the sound cue is presented 3.5 s after the target's disappearance, whereas in the long delay condition the presentation of the sound cue take place 10 s after the target's disappearance. In all there conditions the target reappears 9 s after the presentation of the cue signal (extended time period). Note that in the visual distractor condition a central distractor (between occluder A and B) is presented (for 2 s) before the cue signal. Error bars represent ±standard error. Figure options Finally, we conducted follow-up analyses to clarify interactions with age-group. One-way ANOVAs on looking time at the correct and incorrect occluder in each time interval, with age group as a between-subjects factor, revealed that the 18-month-olds looked more at the incorrect occluder in the first time interval (0–3 s), and less at the correct occluder in all time intervals (0–3 s, 3–6 s, 6–9 s) compared to the adults, Fs > 7.23 and ps < .009. No significant difference was found between the age groups in looking time at the incorrect occluder in the last two time intervals (3–6 s, 6–9 s), Fs < 2.79, ps > .098 (see Fig. 4).