1. Introduction
Children and adolescents with neurological disorders (e.g., neuromuscular disorders, cerebral palsy, traumatic brain injury) are often diagnosed with attention deficit hyperactivity disorder (ADHD) [
1]. One of the symptoms, as described in the DSM-5 [
2], is susceptibility to distraction. In a recent study, Forster and Lavie [
3] proposed “an attention-distractibility trait” underlying this and other ADHD symptoms. These researchers presented data of healthy adults showing a positive association between the degree of task-irrelevant distractor interference (i.e., the observed slowing of visual reaction times caused by distracting stimuli that have no relation to the task at hand) and childhood ADHD symptom severity reported retrospectively. However, these results could not be replicated [
4]. Nevertheless, these results show that distraction by task-irrelevant stimuli can be quantified as a specific attentional process. Assessment of task-irrelevant distraction during cognitive attention tasks contribute to the psychometric sensitivity of these tasks and may potentially be useful in the diagnosis and management of ADHD [
5,
6].
Traditionally, attentional processes during cognitive tasks are quantified in terms of the speed and accuracy with which task-relevant stimuli (i.e., stimuli that have to be processed for adequate completion of the task at hand) are processed and reacted upon. Similarly, in previous studies, assessment of distractibility is based on the speed and accuracy of information processing during task-irrelevant distraction [
3,
4,
5,
6]. Since the visual information that is actively processed can be derived from the direction of gaze [
7,
8,
9], recording eye movements during visual distraction would provide a directly observable and therefore valid measure of the susceptibility to distraction. It can be argued that analysis of gaze behavior using eye tracking during cognitive tasks can provide deeper insight into the occurring attentional processes, including task-irrelevant distraction [
10,
11].
Two recent studies on this topic in adults showed enhanced correct ADHD classification rates for a validated task-irrelevant distractor test when gaze distribution information was added to the conventional outcome measures (i.e., speed and accuracy of information processing) [
12,
13]. These results were most prominent when visual distractors were used as compared to auditory distractors. This emphasizes the necessity of taking into account the effect of distractor modalities on the diagnostic effectiveness of such tests. At the level of visual distraction, it is important to take into account the possible mediating effects of visual distractor appearance. The visual properties and semantic properties (i.e., the meaningfulness in the context of daily life) of distractors used in distraction tests may influence the effectiveness of these tests (visual properties: [
14,
15], semantic properties: [
11,
16,
17,
18,
19]).
Assessment of gaze behavior using eye tracking may contribute to a better understanding of distractibility in children with ADHD or neurological disorders. ADHD is presented as a heterogeneous clinical disorder, with patients presenting varying cognitive and behavioral symptoms [
20]. Valid assessment of distractibility as a specific cognitive symptom of ADHD may therefore contribute to diagnosis, treatment, and management of symptoms in children with ADHD or neurological disorders in daily life. Analysis of gaze behavior through eye tracking during cognitive tasks has already proven to be beneficial in the understanding of attentional processes within a variety of disorders in children and adolescents (Autism [
21]; Anxiety [
22]; ADHD [
23]). Furthermore, using eye movements instead of manual motor output in the assessment of attentional processes would make cognitive tasks suitable to a larger group of individuals with neurological disorders and motor disabilities (e.g., neuromuscular disorders).
In the current study, we aimed to assess the clinical utility and validity of an eye-tracking-based cognitive task (IDistrack) we developed to assess the susceptibility of children to task-irrelevant distraction. In the first part of the study, we compared gaze behavior and manual press latencies during task-irrelevant distractor interference between children and adolescents with a formal ADHD diagnosis or neurological disorders and their non-ADHD or typically developing peers, respectively. We also assessed the association between gaze behavior data and parent-reported attention problems. In the second part of the study, we assessed the effects of distractor modality (i.e., auditory distractors, visual distractors with low semantic salience, visual distractors with high semantic salience, and combinations between the visual and auditory modalities) on the degree of task-irrelevant distraction. We hypothesize children and adolescents with ADHD or a neurological disorder to be most susceptible to task-irrelevant distraction and that the degree of task-irrelevant distraction is most prominent when visual distractors with high semantic salience are used.
3. Results
3.1. Inclusion Criteria for Statistical Analysis
Eye tracking data of participants were included for analyses based on data quality and comprehension of instruction. These parameters were quantified as the percentage of total gaze samples collected and the number of spacebar presses. To include reliable gaze responses, a cut-off point for the percentage of gaze samples was set at 50% based on visual inspection. The cut-off point for average number of spacebar presses per presentation sequence was established on 20 presses based on the maximum presence of 16 events per sequence (8 target color changes and 8 distractor events). This means that in case the participant pressed the spacebar after all target events and all distractor events, data are still included for analysis. These criteria resulted in the exclusion of 36 of the total of 177 participants: 16 of the 37 SE children (43%), 18 of the 113 NLD children (16%), and 2 of the 27 TD children (7%). The mean age (M = 7.50, SD = 2.24) and mean IQ (M = 78.32, SD = 19.10) of the excluded participants were significantly lower compared to the participants that were included for further analysis (Age: W = 1112, p < 0.001; IQ: W = 916, p = 0.01)
3.2. Homogeneity of Subgroups
A non-parametric Mann–Whitney test was conducted to check for differences in age between the ADHD and non-ADHD subgroups. No significant difference was found (W = 1928,
p = 0.30). Chi-squared tests for homogeneity show an unequal distribution of gender over the ADHD subgroups (Χ
2 (1,
n = 141) = 3.99,
p = 0.046) and an equal distribution of psychoactive medication (X
2(1,
n = 141) < 0.001,
p = 1). Available IQ scores for participants with ADHD (M = 87.64, SD = 13.21,
n = 36) and without an ADHD diagnosis (M = 88.55, SD = 16.17,
n = 58) are similar (Mann–Whitney test: W = 1136,
p = 0.48). See
Table 1 for an overview of the demographics after inclusion for analysis.
A non-parametric Kruskal–Wallis test was conducted to check for differences in age between the SE, NLD, and TD subgroups. Besides the mean age of the NLD participants being significantly higher than the TD participants (H(2) = 6.59, p = 0.04), these subgroups did not differ in age. Chi-squared tests for homogeneity show an equal distribution of gender over the SE, NLD, and TD subgroups (Χ2 (2, n=141) = 0.01, p = 0.995) but no equal distribution of ADHD diagnoses (X2 (2, n = 141) = 11.93, p = 0.003) and no equal distribution of psychoactive medication intake (X2 (2, n = 141) = 20.66, p < 0.001). IQ testing of the NLD and SE neurological disorder subgroups revealed a low average IQ for both groups (NLD: M = 89.42, SD = 15.14, n = 74; SE: M = 83.70, SD = 14.20, n = 20), and no significant difference was found (Mann–Whitney test: W = 574, p = 0.13). The TD group is assumed to have an average IQ, as they attended regular schooling and no IQ data were available for this group.
3.3. IDistrack Outcome Measures in Relation to a Clinical ADHD Diagnosis
3.3.1. Time in Area of Interest (tAOI)
A significant main effect of ADHD diagnosis was found (F
ATS = 5.01,
p = 0.025), indicating that children diagnosed with ADHD spent less time looking in the AOI, compared to their non-ADHD peers (
Figure 3). Additionally, a significant main effect of distractor modality on tAOI was found (F
ATS = 92.33,
p < 0.001). Post hoc non-parametric pairwise comparisons show that the Cartoon and the combined Cartoon–Audio modalities correspond to significantly lower scores than all other modalities (
p < 0.001 for all comparisons). No significant interaction effect of ADHD diagnosis by distractor modality was found (F
ATS = 0.58,
p = 0.66).
3.3.2. Press Latencies (PL)
No significant main effect of ADHD diagnosis on PL was found (F
ATS = 0.07,
p = 0.79), indicating that children with and without ADHD had equal manual press latencies (
Figure 4). A significant main effect of the Distractor modality on PL was found (F
ATS = 5.69,
p < 0.001). Post hoc non-parametric comparisons show significantly higher manual press latencies for the Cartoon modality compared to all other modalities without Bonferroni correction (
p < 0.05 for all comparisons). After Bonferroni correction for multiple testing, only the difference with the combined Smiley–Audio modality became non-significant. No significant interaction effect of ADHD diagnosis by distractor modality was found (F
ATS = 0.74,
p = 0.57).
3.4. IDistrack Outcome Measures in Relation to Neurological Disorder
3.4.1. Time in Area of Interest (tAOI)
A significant main effect of subgroup on tAOI was found (F
ATS = 24.01,
p < 0.001). Post hoc non-parametric pairwise comparisons show that the TD group spent significantly more time in the AOI compared to the NLD group and the SE group. Furthermore, the NLD group spent significantly more time in the AOI than the SE group (
p < 0.001 for all comparisons; see
Figure 3). Additionally, a significant main effect of distractor modality on tAOI was found (F
ATS = 86.69,
p < 0.001). Non-parametric post hoc pairwise comparisons show that, irrespective of subgroup, the participants spent significantly less time looking in the AOI when Cartoon distractors or combined Cartoon–Audio distractors were presented, compared to all other distractor modalities (
p < 0.001 for all comparisons). This indicates that irrespective of participant subgroup, visual distractors with high semantic salience have the strongest distracting effect. The results show no significant interactions of participant subgroup by distractor modality (F
ATS = 0.66,
p = 0.67).
3.4.2. Press Latencies (PL)
A significant main effect of subgroup on PL was found (F
ATS = 7.63,
p < 0.001). Post hoc non-parametric pairwise comparisons show that the TD group had significantly lower manual press latencies compared to the NLD group and the SE group. Furthermore, the NLD group had significantly lower manual press latencies than the SE group (
p < 0.01 for all comparisons; see
Figure 4). Additionally, a significant main effect of distractor modality on PL was found (F
ATS = 4.80,
p < 0.001). Post hoc non-parametric pairwise comparisons show that manual press latencies for the Cartoon modality were significantly higher than for the other modalities, but after Bonferroni correction, the difference with the combined Smileys–Audio modality became non-significant. The results show no significant interactions of participant subgroup by distractor modality (F
ATS = 1.37,
p = 0.21).
3.5. Correlation of Eye Movement Responses with Parent-Reported Attention Problems
The associations between tAOI of the most effective distractor modalities causing the most task-irrelevant distraction (Cartoons and combined Cartoon–Audio) and a validated behavioral questionnaire assessing parent-reported attention problems (CBCL) were analyzed. Data of the CBCL parent-reported questionnaire were available for participants in the NLD and TD subgroups (n = 88). The results show significant negative Spearman’s correlations between the classification score on the CBCL Attention Problems subscale (i.e., a T-score corresponding to a normal, borderline, or clinical classification of attention problems) and tAOI in the Cartoon modality (rs = −0.36, p < 0.001, n = 88) and the combined Cartoon–Audio modality (rs = −0.39, p < 0.001, n = 88).
4. Discussion
To the best of our knowledge, this is the first study reporting on a computer-assisted assessment paradigm for children and adolescents of six years and older assessing task-irrelevant distraction on the basis of eye tracking data. We developed an easy-to-administer, simple, and efficient computerized testing procedure, wherein manual press latency and eye movements are recorded during visual and auditory distraction in a simple visual reaction time task. The testing procedure requires minimal verbal instruction and requires minimal manual motor output from the participants. This makes the test procedure suitable for a wide range of children and adolescents with both minor and major motor disabilities.
When comparing the gaze behavior of the subgroups during the IDistrack task, the results are as expected: children and adolescents with ADHD show more distractibility compared to children and adolescents without ADHD. Furthermore, similar differentiation is found between the subgroups based on the presence of neurological disorders: children and adolescents with neurological disorders show more distractibility compared to typically developing individuals. These findings are in line with the elevated comorbidity rates of attention deficit disorders in children and adolescents with neurological disabilities [
1].
Our data show a spectrum of distractibility problems that are similar to those described by Forster and Lavie [
3]. This implies that distractibility may be clinically presented in children with ADHD and in children with neurological disorders as a dysfunctional attentional process. However, in our study this is only consistently reflected in the gaze behavior, as we did not observe the expected differences in manual press latencies between the ADHD and non-ADHD group. This underlines the clinical utility and added value of recording eye movements in this clinical population.
Regarding the different distractor modalities, the results are partly as expected. Cartoon distractors (which have a high semantic load and are semantically meaningful in the context of daily life: e.g., a tree or a bike) caused the most distraction compared to auditory distractors and visual distractors with low semantic load (e.g., a single-color smiley shape). This is in line with previous attempts with eye-tracking-based distractor paradigms in an adult population [
12,
13] and literature on task-irrelevant distraction [
16,
17,
18,
19]. In our study, participants with ADHD or neurological disabilities were not disproportionately affected by changes in distractor modality as no interaction effects were found. Nevertheless, IDistrack outcome measures for the semantically meaningful Cartoon modality show a significant, moderate association with parent-reported attention problems (CBCL). Semantically meaningful distractors are therefore sensitive in the assessment of distractibility through eye tracking.
Based on the results of our study, we conclude that eye tracking during a task-irrelevant distractor paradigm is a feasible, efficient, and valid method for the measurement of distractibility in children. Evidence of elevated levels of distractibility in children with attention deficit disorders or neurological disorders is provided. These findings contribute to the notion of an attention-distractibility trait that is clinically relevant in the assessment of cognitive attention problems in children, and that assessment of distractibility should be taken into account in neuropsychological evaluations of children and adolescent with neurological disorders. The IDistrack paradigm has been shown in the current study to be a suitable and valid paradigm for clinical assessment of distractibility. Eye distraction data may enhance the diagnostic precision of a neuropsychological assessment for the assessment of ADHD in children and adolescents. Further research is needed.
4.1. Limitations
The current study may have several shortcomings. First, the IDistrack paradigm lacks an initial set of trials without the presence of distractors that serves as a baseline measurement for manual press latency. Comparing manual press latencies during IDistrack with this baseline would enhance the validity by eliminating confounding factors, such as cognitive processing speed. Second, because of the selection of patients with epilepsy, a considerable proportion (29%) of the SE group used anti-epileptic drugs (AEDs) during the administration of the IDistrack task. Cognitive side-effects of the AEDs could have been a confounding factor by causing high press latencies in this group [
26]. Moreover, possible epileptic events (e.g., absences) during task administration were not recorded. For the ADHD and non-ADHD groups, psychoactive drug intake was equally distributed and no significant differences in manual press latency were found. Third, the cut-off point for minimal eye tracking data quality was set at a maximum of 50% gaze data loss during task administration. Though these amounts of data loss are acceptable for the current research purposes [
27], this cut-off point remains arbitrary.
4.2. Future Research
Further research is needed on the clinical utility of this procedure. In order to obtain normative scores for the purpose of discriminating between normal and disturbed distractibility levels, data on a larger group of children need to be collected and the effects of age on distractibility need to be investigated [
28]. Furthermore, the clinical relevance of the paradigm should be investigated by comparing eye tracking data in children with ADHD during an off and on period of attention-regulating medication. This may be a simple and quick method for medication monitoring in ADHD and needs further research. Our research group is currently collecting these data. Further research on the reliability, criterion validity, and construct validity in a greater group of typically developing children and children with neurological disorders should be conducted in order to establish the psychometric quality of the IDistrack task. For this purpose, we suggest enhancing the current IDistrack task by adding a baseline measurement without distraction before starting the distraction procedure, using only visual distractors that are meaningful in the context of daily life.