Eyes on CVI: Eye movements unveil distinct visual search patterns in Cerebral Visual Impairment compared to ADHD, dyslexia, and neurotypical children.

Visual search problems are often reported in children with Cerebral Visual Impairment (CVI). To tackle the clinical challenge of objectively differentiating CVI from other neurodevelopmental disorders, we developed a novel test battery. Visual search tasks were coupled with verbal and gaze-based measurements. Two search tasks were performed by children with CVI (n: 22; mean age (SD): 9.63 (.46) years) ADHD (n: 32; mean age (SD): 10.51 (.25) years), dyslexia (n: 28; mean age (SD): 10.29 (.20) years) and neurotypical development (n: 44; mean age (SD): 9.30 (.30) years). Children with CVI had more impaired search performance compared to all other groups, especially in crowded and unstructured displays and even when they had normal visual acuity. In-depth gaze-based analyses revealed that this group searched in overall larger areas and needed more time to recognize a target, particularly after their initial fixation on the target. Our gaze-based approach to visual search offers new insights into the distinct search patterns and behaviours of children with CVI. Their tendency to overlook targets whilst fixating on it, point towards higher-order visual function (HOVF) deficits. The novel method is feasible, valid, and promising for clinical differential-diagnostic evaluation between CVI, ADHD and dyslexia, and for informing individualized training.

Parent-reported problems in children with Cerebral Visual Impairment: Improving the discriminative ability from ADHD and dyslexia using screening inventories.

Daily problems of children with Cerebral Visual Impairment (CVI) are often misinterpreted as symptoms of behavioural disorders or learning disabilities instead of higher order visual function (HOVF) deficits. It is difficult to differentiate between various paediatric clinical groups based on daily manifestations. We used two CVI inventories (V-CVI-I, HVFQI) and an ADHD questionnaire (AVL) to compare parent-reported visual and behavioural problems of children with CVI, ADHD, dyslexia and neurotypical children (Age 6-15, Verbal Intelligence > 70). Our results show a higher percentage of parent-reported visual problems in children with CVI compared to all other groups, which was not affected by their visual acuity levels. On most HOVF categories, a higher percentage of parent-reported visual problems was also found in children with ADHD or dyslexia compared to neurotypical children. Children with ADHD had significantly more parent-reported behavioural problems, but more behavioural problems were reported by the parents of children with CVI compared to neurotypical children as well. Our findings complicate using the existing inventories for initial screening and referral of children with potential CVI. We propose a shortened screening list to improve the potential differentiation between CVI and ADHD or dyslexia based on parent-reported visual problems in everyday life.

[Formula: see text] Visual selective attention and visual search performance in children with CVI, ADHD, and Dyslexia: a scoping review.

Visual selective attention refers to the selection of relevant visual elements in a scene whilst ignoring irrelevant visual elements. Visual Selective Attention Dysfunctions (VSAD) are prevalent in children with Cerebral Visual Impairment (CVI), Attention Deficit Hyperactivity Disorder (ADHD), and Dyslexia. An important issue in the pediatric neuropsychological practice is how to discriminate between the task performance of these populations. We conducted a scoping review of the literature on visual search performance (VSP) in children with CVI, ADHD, and Dyslexia, aged 6-12 years. After a systematic selection process, 35 studies were included. Results suggest that all patient groups have some degree of impaired VSP compared to typically developing children. Children with CVI tend to react slower and less accurately. VSP impairments in children with ADHD are characterized by poor accuracy rather than reaction time. Children with Dyslexia tend to be slower and less accurate, depending on stimulus type. Besides VSAD, it is argued that other neurocognitive mechanisms might influence VSP, such as speed-accuracy trade-off or an executive functioning deficit in ADHD and a phonological deficit in Dyslexia. This paper further discusses the differences and similarities in visual search performance between the groups. The sparse data in children with an official diagnosis of CVI and the technical inconclusive data on children with ADHD and Dyslexia demonstrate complexity of discriminating between these populations in clinical practice based on VSP. New and more quantitative VSP parameters, such as eye tracking-based measures, may contribute to a refined classification among CVI, ADHD, and Dyslexia.

Clinical Utility of Eye Tracking in Assessing Distractibility in Children with Neurological Disorders or ADHD: A Cross-Sectional Study.

This study aims to investigate distractibility quantified by recording and analyzing eye movements during task-irrelevant distraction in children with and without ADHD and in children with and without neurological disorders. Gaze behavior data and press latencies of 141 participants aged 6−17 that were collected during a computerized distraction paradigm with task-irrelevant stimuli (IDistrack) were analyzed. Children using attention-regulating medication were excluded from participation. Data were analyzed for subgroups that were formed based on the presence of neurological disorders and the presence of ADHD separately. Participants with ADHD and participants with neurological disorders spent less time fixating on the target stimuli compared to their peers without ADHD (p = 0.025) or their peers without neurological disorders (p < 0.001). Participants with and without ADHD had equal press latencies (p = 0.79). Participants with neurological disorders had a greater press latency compared to their typically developing peers (p < 0.001). Target fixation duration shows a significant association with parent-reported attention problems (r = −0.39, p < 0.001). We conclude that eye tracking during a distraction task reveals potentially valid clinical information that may contribute to the assessment of dysfunctional attentional processes. Further research on the validity and reliability of this paradigm is recommended.

Early Screening of Visual Processing Dysfunctions in Children Born Very or Extremely Preterm.

Introduction: Children with early brain damage or dysfunction are at risk of developing cerebral visual impairment (CVI), including visual processing dysfunctions (VPD), which currently remain largely undetected until school age. Our aim was to systematically screen for possible VPD in children born very or extremely preterm from 1 to 2 years corrected age (CA) and to evaluate the effectiveness of early referral. Method: We included N = 48 children born < 30 weeks from 1 year CA. They underwent a two-step VPD screening based on (1) neurological signs indicative of visual brain damage evaluated by neonatologists and/or pediatric neurologist and (2) a functional assessment of visual orienting functions (VOF) with an eye tracking-based test. If at least one of these assessments was abnormal for their age, the children were classified as a risk of VPD and referred to undergo conventional visual diagnostics: ophthalmic exam and visual function assessment (VFA). At 2 years CA, VOF screening was repeated and neurodevelopment was assessed. Results: 18 children (38%) were classified as at risk of VPD at 1 year CA. 7 children had abnormal neurological signs, 5 children had abnormal VOF, and 6 children had both. Subsequent ophthalmic exams (N = 14) showed severe hypermetropia in 21% and strabismus in 14%. VFA (N = 10) showed abnormal visual function and behavior in only 1 child. At 2 years CA, the total group showed an increase in abnormal VOF. Whereas the children at risk showed some normalization, the group without VPD risk at 1 year CA showed deterioration of VOF. Neurodevelopmental outcome did not clearly differ between risk groups. Conclusion: Our findings show a substantial risk of VPD during visual screening (in 38%) at 1 year CA, but relatively few deficits on subsequent conventional ophthalmic exams and VFA. The data suggest that most conventional visual diagnostic methods at this young age are not related to the established VPD risks. VOF assessment should be used complimentary to these methods. The fact that at 2 years CA the number of children with a VPD risk based on abnormal VOF increased argues for more extensive and continuous screening in risk groups, at least until school age.

Early visuospatial attention and processing and related neurodevelopmental outcome at 2 years in children born very preterm.

BACKGROUND: The ability to perceive and process visuospatial information is a condition for broader neurodevelopment. We examined the association of early visuospatial attention and processing with later neurodevelopmental outcome in very preterm infants. METHODS: Visuospatial attention and processing was assessed in 209 children (<30 weeks gestation) using an easy applicable eye tracking-based paradigm at 1 and 2 years. Average reaction times to fixation (RTF) on specific visual stimuli were calculated, representing time needed for overall attention (Cartoon stimuli) and processing (Motion and Form stimuli). Associations between RTFs and various measures of development at 2 years including cognitive and motor development (Bayley Scales of Infant and Toddler Development-Third edition; Bayley-III), language (Lexi test) and behavior (Child Behavior Checklist) were examined. RESULTS: At 1 year, 100 ms slower Cartoon and Motion RTFs were associated with lower cognitive Bayley-III scores (-4.4 points, 95%CI: -7.4; -1.5 and -1.0 points, -1.8; -0.2, respectively). A 100 ms slower Cartoon RTF was associated with a 3.5 (-6.6; -0.5) point decrease in motor Bayley-III score. CONCLUSIONS: Visuospatial attention and motion processing at 1 year is predictive of overall cognitive and motor development 1 year later. The nonverbal eye tracking-based test can assist in early detection of preterm children at risk of adverse neurodevelopment. IMPACT: Visuospatial attention and processing at 1 year corrected age is predictive for overall cognitive and motor development 1 year later in preterm infants. First study to relate early visuospatial attention and processing with later neurodevelopmental outcome in preterm children. Early detection of preterm children at risk of adverse neurodevelopment, which allows for more timely interventions.

Brain Damage and Visuospatial Impairments: Exploring Early Structure-Function Associations in Children Born Very Preterm.

BACKGROUND: To provide insight into early neurosensory development in children born very preterm, we assessed the association between early structural brain damage and functional visuospatial attention and motion processing from one to two years corrected age. METHODS: In 112 children born at less than 32 weeks gestational age, we assessed brain damage and growth with a standardized scoring system on magnetic resonance imaging (MRI; 1.5 Tesla) scans performed at 29 to 35 weeks gestational age. Of the children with an MRI scan, 82 participated in an eye tracking-based assessment of visuospatial attention and motion processing (Tobii T60XL) at one year corrected age and 59 at two years corrected age. RESULTS: MRI scoring showed good intra- and inter-rater reproducibility. At one year, 10% children had delayed attentional reaction times and 23% had delayed motion reaction times. Moderate to severe brain damage significantly correlated with slower visuospatial reaction times. At two years, despite attention and motion reaction times becoming significantly faster, 20% had delayed attentional reaction times and 35% had delayed motion reaction times, but no correlations with MRI scores were found. The presence of structural brain damage was associated with abnormal functional performance over age. CONCLUSIONS: The present study indicates an association between moderate to severe brain damage and visuospatial attention and motion processing dysfunction at one year corrected age. This provides a new perspective on comprehensive MRI scoring and quantitative functional visuospatial assessments and their applicability in children born very preterm in their first years of life.

Early intervention for children at risk of visual processing dysfunctions from 1 year of age: a randomized controlled trial protocol.

BACKGROUND: An increasing number of children are suffering from brain damage-related visual processing dysfunctions (VPD). There is currently a lack of evidence-based intervention methods that can be used early in development. We developed a visual intervention protocol suitable from 1 year of age. The protocol is structured, comprehensive and individually adaptive, and is paired with quantitative outcome assessments. Our aim is to investigate the effectiveness of this first visual intervention program for young children with (a risk of) VPD. METHODS: This is a single-blind, placebo-controlled trial that is embedded within standard clinical care. The study population consists of 100 children born very or extremely preterm (< 30 weeks) at 1 year of corrected age (CA), of whom 50% are expected to have VPD. First, children undergo a visual screening at 1 year CA. If they are classified as being at risk of VPD, they are referred to standard care, which involves an ophthalmic and visual function assessment and a (newly developed) visual intervention program. This program consists of a general protocol (standardized and similar for all children) and a supplement protocol (adapted to the specific needs of the child). Children are randomly allocated to an intervention group (starting upon inclusion at 1 year CA) or a control group (postponed: starting at 2 years CA). The control group will receive a placebo treatment. The effectiveness of early visual intervention will be examined with follow-up visual and neurocognitive assessments after 1 year (upon completion of the direct intervention) and after 2 years (upon completion of the postponed intervention). DISCUSSION: Through this randomized controlled trial we will establish the effectiveness of a new and early visual intervention program. Combining a general and supplement protocol enables both structured comparisons between participants and groups, and custom habilitation that is tailored to a child's specific needs. The design ensures that all included children will benefit from participation by advancing the age at which they start receiving an intervention. We expect results to be applicable to the overall population of children with (a risk of) VPD early in life. TRIAL REGISTRATION: Netherlands Trial Register: NTR6952. Registered 19 January 2018.

Gestalt Perception in Children With Visual Impairments: Item-Specific Performance and Looking Behavior.

Visual closure is the ability to visualize a complete whole when an incomplete picture is presented. The aim of the present study was to investigate the Kaufman Gestalt closure task in children with cerebral and ocular visual impairments. Looking behavior was assessed by an eye tracker system to quantify the number and duration of fixations. We found that children with visual impairments due to cerebral damage show weaker Gestalt perception and had different looking patterns than children with ocular or without visual impairments. Children with brain damage performed significantly worse on the animate items than the group without brain damage.

Combining visual sensory functions and visuospatial orienting functions in children with visual pathology: A longitudinal study.

BACKGROUND: Peripheral and central visual processing development highly depends on the integrity of the visual sensory system and the allocation of visuospatial attention. METHOD: We quantitatively followed visual sensory functions (VSF) and visuospatial orienting functions (VOF) over two years in 77 children (1-13 years) with different types of visual pathology. RESULTS: Within the clinical groups, VSF were relatively constant over two years, except visual acuity, and VOF were characterized by longer reaction time, shorter fixation duration, and lower fixation accuracy than normal for their age. Children with peripheral pathology had high rates of abnormal VSF, of changes to abnormal visual acuity at 1-6 years, and larger and more abnormal VOF (fixation inaccuracy). Children with central pathology had relatively good VSF, whereas two-third had delayed orienting reaction times that differed from other groups mainly at 1-6 years. CONCLUSION: The distinct patterns of quantitative VSF and VOF over time between the visual pathology groups, and the finding that both methods provided complementary information, argues for combining both types of assessments to provide comprehensive monitoring of visual functioning in children from a young age.

A Method to Quantify Visual Information Processing in Children Using Eye Tracking.

Visual problems that occur early in life can have major impact on a child's development. Without verbal communication and only based on observational methods, it is difficult to make a quantitative assessment of a child's visual problems. This limits accurate diagnostics in children under the age of 4 years and in children with intellectual disabilities. Here we describe a quantitative method that overcomes these problems. The method uses a remote eye tracker and a four choice preferential looking paradigm to measure eye movement responses to different visual stimuli. The child sits without head support in front of a monitor with integrated infrared cameras. In one of four monitor quadrants a visual stimulus is presented. Each stimulus has a specific visual modality with respect to the background, e.g., form, motion, contrast or color. From the reflexive eye movement responses to these specific visual modalities, output parameters such as reaction times, fixation accuracy and fixation duration are calculated to quantify a child's viewing behavior. With this approach, the quality of visual information processing can be assessed without the use of communication. By comparing results with reference values obtained in typically developing children from 0-12 years, the method provides a characterization of visual information processing in visually impaired children. The quantitative information provided by this method can be advantageous for the field of clinical visual assessment and rehabilitation in multiple ways. The parameter values provide a good basis to: (i) characterize early visual capacities and consequently to enable early interventions; (ii) compare risk groups and follow visual development over time; and (iii), construct an individual visual profile for each child.

Quantification of visual function assessment using remote eye tracking in children: validity and applicability.

PURPOSE: Measurements of visual and oculomotor functions are essential for providing tailored support to visually impaired children. In young or intellectually disabled children these measurements can be difficult or even impossible to perform. Recordings of orienting gaze in response to specific visual information, made with eye tracking, may offer a solution. The aim of this study was to observe and quantify eye tracking (ET)-based gaze responses to provide information about visual and oculomotor functioning, and to compare this information with standard visual function assessments (VFA). METHODS: One hundred and twenty-six visually impaired children from 1-14 years underwent a VFA. Next they underwent a remote ET test. Four aspects of oculomotor control (nystagmus, fixation, saccades, pursuit) and three visual functions (visual field, contrast, colour) were selected to compare both methods. Performance was assessed (1) during VFA using standard behavioural observation and test scores and (2) after ET by observing and scoring the eye movement recordings. Validity, in terms of agreement between results, was measured by correlation analyses. From the orienting gaze responses, quantitative parameters (gain, fixation duration and directional saccades) were calculated to characterize visual performance. RESULTS: Good agreement between the two test methods was found for observational assessment of oculomotor control and visual functions (correlations ranging from rs  = 0.39 to rs  = 0.69). The quantitative parameters of visual performance showed distinct results between children with and without specific functional impairments, both in children aged 1-6 and 7-14 years. CONCLUSION: Eye tracking-based gaze recordings are a promising tool to assess oculomotor and visual performance in a communication-free manner. Calculating quantitative parameters from specific gaze responses could assist in the characterization of functional visual performance in children, independent of age. Gaze responses are a useful addition to standard VFA in clinical practice.

Development of salience-driven and visually-guided eye movement responses.

Development of visuospatial attention can be quantified from infancy onward using visually-guided eye movement responses. We investigated the interaction between eye movement response times and salience in target areas of visual stimuli over age in a cohort of typically developing children. A preferential looking (PL) paradigm consisting of stimuli with six different visual modalities (cartoons, contrast, form, local motion, color, global motion) was combined with the automated measurement of reflexive eye movements. Effective salience was defined as visual salience of each target area relative to its background. Three classes of PL stimuli were used: with high- (cartoon, contrast), intermediate- (local motion, form), and low-effective salience (global motion, color). Eye movement response times to the target areas of the six PL stimuli were nonverbally assessed in 220 children aged 1-12 years. The development of response times with age was influenced by effective salience: Response times to targets with high salience reached stable values earlier in development (around 4 years of age) than to targets with low salience (around 9 years of age). Intra-individual response time variability was highest for low-salient stimuli, and stabilized later (around 4 years) than for highly salient stimuli (2 years). The improvement of eye movement response times to visual modalities in PL stimuli occurred earlier in development for highly salient than for low-salient targets. The present age-dependent and salience-related results provide a quantitative and theoretical framework to assess the development of visuospatial attention, and of related visual processing capacities, in children from 1 year of age.

The relationship between visual orienting responses and clinical characteristics in children attending special education for the visually impaired.

We recently introduced a method based on quantification of orienting responses toward visual stimuli to assess the quality of visual information processing in children. In the present study, we examined the relationship between orienting responses and factors that are associated with visual processing impairments in current clinical practice. Response time and fixation quality to visual features such as form, contrast, motion, and color stimuli were assessed in 104 children from 1 to 12 years attending special education for the visually impaired. Using regression analysis, we investigated whether these parameters were affected by clinical characteristics of children. Response times significantly depended on stimulus type. Responses to high-contrast cartoons were significantly slower in children with a clinical diagnosis of cerebral visual impairment. Fixation quality was significantly affected by visual acuity and nystagmus. The results suggest that the quantitative measurement of orienting responses is strongly related to cerebral visual impairment in children.

Reliability of visual orienting response measures in children with and without visual impairments.

BACKGROUND: From the need for a quantitative method to examine visual processing in young children, we measured ocular orienting responses to visual stimuli (form, motion, expansion, color, contrast, cartoons). Reliability and applicability of this method were assessed. NEW METHOD: 80 children (1-12 years) with visual impairments and a reference group of 118 typically developing children (1-6 years) completed two sessions. Test-retest reliability was measured by calculating differences in reaction time and fixation accuracy between the two sessions. For applicability, the cumulative percentage of children that fell within a pre-defined reliability interval was plotted against the mean number of responses. RESULTS: In typically developing children none of the outcome measures significantly differed between sessions. In the children with visual impairments similar results were obtained, except for motion. This stimulus elicited significantly faster reaction times in the second session. In at least 80% of the children reliable reaction times could be calculated if 4 responses to a cartoon stimulus and 1 or 2 responses to the other stimuli were measured. COMPARISON WITH EXISTING METHOD(S): The existing method to quantify visual information processing has been refined: the range of visual functions was extended and a criterion for reliable assessment of orienting response times was established. CONCLUSIONS: Objective measurement of orienting responses is a reliable method to test the initial stage of visual processing in children with and without visual impairments. A set minimum number of responses for each stimulus warrants the reliability of measurements obtained with this functional method in clinical practice.