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Eye Movements to Evaluate and Treat Attention Deficits

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A special issue of Brain Sciences (ISSN 2076-3425). This special issue belongs to the section "Neuro-otology and Neuro-ophthalmology".

Deadline for manuscript submissions: closed (15 April 2022) | Viewed by 26210

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Dr. Zoi Kapoula

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1. CNRS Research Director, Neurosciences, LIPADE Laboratory, University of Paris, 75006 Paris, France
2. Leader of the Research Group Eye Analytics & Rehabilitation, Orasis-EAR, 75015 Paris, France
Interests: eye movements; dyslexia; strabismus; tinnitus; vestibular deficits; cognitive impairment
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Special Issue Information

Dear Colleagues,

There is a long history of interest in eye movements for evaluating attention. Eye movement training is also broadly used in clinics, empirically most of the time. This issue is devoted to studies presenting research-based clinical evaluation of attention via eye movements and training of attention via eye movements in various pathologies.

Topics of interest include which eye movements, what parameters, and what types of analysis (hypothesis-based vs. data-driven) reflect best attention inefficiency or deficits during development, aging, or neurologic pathologies, as well as how and which type of eye movement training can improve attention efficiency in patients. Emphasis will be on clinical and translational research covering a broad panel of clinical issues, such as developmental disorders (dys, attention deficit, autism); neurological disorders such as Parkinson’s; Strokes spatial neglect, visual, cognitive, and auditory impairment; vertigo; and any other pathology in the neuro-otology and neuro-ophthalmology field.

Dr. Zoi Kapoula
Guest Editor

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Published Papers (11 papers)

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Research

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22 pages, 2108 KiB

Open AccessArticle

Attentional Engagement and Disengagement Differences for Circumscribed Interest Objects in Young Chinese Children with Autism

by Li Zhou, Li Zhang, Yuening Xu, Fuyi Yang and Valerie Benson

Brain Sci. 2022, 12(11), 1461; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12111461 - 28 Oct 2022

Cited by 1 | Viewed by 1414

Abstract

The current study aimed to investigate attentional processing differences for circumscribed interest (CI) and non-CI objects in young Chinese children with autism spectrum condition (ASC) and typically developing (TD) controls. In Experiment 1, a visual preference task explored attentional allocation to cartoon CI and non-CI materials between the two groups. We found that ASC children (n = 22, 4.95 ± 0.59 years) exhibited a preference for CI-related objects compared to non-CI objects, and this effect was absent in the TD children (n = 22, 5.14 ± 0.44 years). Experiment 2 utilized the traditional gap-overlap paradigm (GOP) to investigate attentional disengagement from CI or non-CI items in both groups (ASC: n = 20, 5.92 ± 1.13 years; TD: n = 25, 5.77 ± 0.77 years). There were no group or stimulus interactions in this study. Experiment 3 adopted a modified GOP (MGOP) to further explore disengagement in the two groups (ASC: n = 20, 5.54 ± 0.95 years; TD: n = 24, 5.75 ± 0.52 years), and the results suggested that exogenous disengagement performance was preserved in the ASC group, but the children with ASC exhibited increased endogenous attentional disengagement compared to TD peers. Moreover, endogenous disengagement was influenced further in the presence of CI-related objects in the ASC children. The current results have implications for understanding how the nature of engagement and disengagement processes can contribute to differences in the development of core cognitive skills in young children with ASC. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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12 pages, 1467 KiB

Open AccessArticle

Eye-Movement Deficits in Seniors with Hearing Aids: Cognitive and Multisensory Implications

by Martin Chavant and Zoï Kapoula

Brain Sci. 2022, 12(11), 1425; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12111425 - 24 Oct 2022

Cited by 1 | Viewed by 1181

Abstract

In recent years, there has been a growing body of literature highlighting the relationship between presbycusis and consequences in areas other than hearing. In particular, presbycusis is linked to depression, dementia, and cognitive decline. Among this literature, the effect of hearing aids, currently the most common method of treating presbycusis, is also a growing research topic. This pilot study aims to explore the effects of hearing aids on the cognitive and multisensory consequences of presbycusis. To that purpose, saccades and vergences eye movements were studied, towards visual and audiovisual targets, of a presbycusis population wearing hearing aids for an average of two years. These measurements were done whether or not participants were wearing their hearing aids. Eye-movement characteristics, particularly latencies (the reaction time taken to initiate an eye movement), allows one to measure attentional and multisensory characteristics. Previous studies showed that presbycusis was linked with an increase of saccade latencies and an improvement in audiovisual interaction capacities, i.e., latencies for audiovisual targets are shorter than those for visual targets. Eye movements are measured and analyzed with REMOBI and AIDEAL technologies. Results show a shortening, with hearing aids, of right saccade latencies to visual targets, suggesting an increase in attention and/or engagement. Yet, saccade latencies are not shorter for audiovisual vs. visual targets alone, neither when wearing hearing aids, nor without. Moreover, convergence latencies are particularly slow for any type of target and with or without hearing aids. The results suggest deficits for audiovisual interactions and the initiation of convergences in that population. These deficits could be part of the factors triggering the need to wear hearing aids. These results therefore show interesting relationships between hearing-aid wearing in a presbycusis population and oculomotricity and invite further research in this area. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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27 pages, 12271 KiB

Open AccessArticle

Predicting Dyslexia in Adolescents from Eye Movements during Free Painting Viewing

by Alae Eddine El Hmimdi, Lindsey M Ward, Themis Palpanas, Vivien Sainte Fare Garnot and Zoï Kapoula

Brain Sci. 2022, 12(8), 1031; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12081031 - 03 Aug 2022

Cited by 1 | Viewed by 1835

Abstract

It is known that dyslexics present eye movement abnormalities. Previously, we have shown that eye movement abnormalities during reading or during saccade and vergence testing can predict dyslexia successfully. The current study further examines this issue focusing on eye movements during free exploration of paintings; the dataset was provided by a study in our laboratory carried by Ward and Kapoula. Machine learning (ML) classifiers were applied to eye movement features extracted by the software AIDEAL: a velocity threshold analysis reporting amplitude speed and disconjugacy of horizontal saccades. In addition, a new feature was introduced that concerns only the very short periods during which the eyes were moving, one to the left the other to the right; such periods occurred mostly during fixations between saccades; we calculated a global index of the frequency of such disconjugacy segments, of their duration and their amplitude. Such continuous evaluation of disconjugacy throughout the time series of eye movements differs from the disconjugacy feature that describes inequality of the saccade amplitude between the two eyes. The results show that both AIDEAL features, and the Disconjugacy Global Index (DGI) enable successful categorization of dyslexics from non-dyslexics, at least when applying this analysis to the specific paintings used in the present study. We suggest that this high power of predictability arises from both the content of the paintings selected and the physiologic relevance of eye movement features extracted by the AIDEAL and the DGI. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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18 pages, 3556 KiB

Open AccessArticle

Creativity, Eye-Movement Abnormalities, and Aesthetic Appreciation of Magritte’s Paintings

by Lindsey M Ward and Zoi Kapoula

Brain Sci. 2022, 12(8), 1028; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12081028 - 03 Aug 2022

Cited by 1 | Viewed by 2326

Abstract

Dyslexic children have been shown to be more creative than their non-dyslexic counterparts. They have also been shown to have an abnormal oculomotor profile while viewing targets in free space, making vergence or saccadic eye movements while reading or when viewing Op art. They show a slower deceleration of their eye movements and a difficulty in coordinating their two eyes to obtain single fused vision in depth. Interestingly, their abnormal oculo-motor profile is exacerbated while reading more difficult texts. Given these differences, we postulate that dyslexics’ increased creativity may be related to their different eye movement control affecting how they perceive the world. Therefore, we decided to measure adolescent dyslexics’ creativity, oculomotor profile, and subjective responses while they viewed three paintings by Magritte. These were chosen to stimulate the perception of hidden conceptual spaces or stimulate conflict between the perception of the figural and textural content. For the first time to our knowledge, dyslexic adolescents were demonstrated to be more creative in terms of flexibility and fluidity than their non-dyslexic peers. Subjectively, while viewing the Magritte paintings, dyslexics reported fewer conceptual spaces and fewer hidden words than their non-dyslexic peers; thus, they confabulated less than non-dyslexics. Dyslexics also demonstrated an abnormal oculomotor profile similar to those that we have shown when reading, viewing randomized targets, and while perceiving illusions of depth in Op art paintings, in that they demonstrated difficulty with disconjugation and abnormalities in their eye velocity profiles. We propose there may be a link between dyslexic increased creativity and their eye movement abnormalities. Similar to reading nonsense text, we propose that Magritte’s contradictory paintings exacerbate dyslexics’ eye movement abnormalities. These eye movement abnormalities while viewing these particular paintings might provide a physiological signature suggesting a contribution of their unusual eye control to their higher creativity scores. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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18 pages, 3293 KiB

Open AccessArticle

Disconjugate Eye Movements in Dyslexic Adolescents While Viewing Op Art: A Creative Handicap?

by Lindsey M. Ward and Zoi Kapoula

Brain Sci. 2022, 12(7), 835; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12070835 - 26 Jun 2022

Cited by 2 | Viewed by 2661

Abstract

Op art was created, in part, to produce illusions of movement. Given that dyslexics have been shown to have impaired visuo-postural axis deficits, it may be possible that dyslexics see illusions different than their non-dyslexic peers. To test this theory, we measured eye movement and posture in 47 dyslexic (18 female, 29 male; mean age 15.4) and 44 non dyslexic (22 female, 22 male; mean age 14.8) adolescents while they viewed three works of art by Op artist Bridget Riley. They then responded to a questionnaire about how they felt while viewing the artworks. Dyslexics demonstrated significantly slower saccades in terms of average velocity that was particularly disturbed in paintings that manipulated depth. Subjectively, dyslexics felt much more destabilized compared to their peers; however, there was not a significant difference in objective postural measurements between the two groups. The sensation of destabilization was positively correlated with appreciation in non-dyslexic adolescents. These subjective results suggest that dyslexics may be more sensitive to movement in depth, which could be related to the instability in vergence movements. Whereas this instability represents a hinderance in relation to reading, it could be an advantage while viewing paintings such as these. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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20 pages, 1298 KiB

Open AccessArticle

Audiovisual Integration for Saccade and Vergence Eye Movements Increases with Presbycusis and Loss of Selective Attention on the Stroop Test

by Martin Chavant and Zoï Kapoula

Brain Sci. 2022, 12(5), 591; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12050591 - 03 May 2022

Cited by 1 | Viewed by 2105

Abstract

Multisensory integration is a capacity allowing us to merge information from different sensory modalities in order to improve the salience of the signal. Audiovisual integration is one of the most used kinds of multisensory integration, as vision and hearing are two senses used very frequently in humans. However, the literature regarding age-related hearing loss (presbycusis) on audiovisual integration abilities is almost nonexistent, despite the growing prevalence of presbycusis in the population. In that context, the study aims to assess the relationship between presbycusis and audiovisual integration using tests of saccade and vergence eye movements to visual vs. audiovisual targets, with a pure tone as an auditory signal. Tests were run with the REMOBI and AIDEAL technologies coupled with the pupil core eye tracker. Hearing abilities, eye movement characteristics (latency, peak velocity, average velocity, amplitude) for saccade and vergence eye movements, and the Stroop Victoria test were measured in 69 elderly and 30 young participants. The results indicated (i) a dual pattern of aging effect on audiovisual integration for convergence (a decrease in the aged group relative to the young one, but an increase with age within the elderly group) and (ii) an improvement of audiovisual integration for saccades for people with presbycusis associated with lower scores of selective attention in the Stroop test, regardless of age. These results bring new insight on an unknown topic, that of audio visuomotor integration in normal aging and in presbycusis. They highlight the potential interest of using eye movement targets in the 3D space and pure tone sound to objectively evaluate audio visuomotor integration capacities. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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21 pages, 11868 KiB

Open AccessArticle

Presbycusis and the Aging of Eye Movement: Common Attention Mechanisms

by Martin Chavant and Zoï Kapoula

Brain Sci. 2022, 12(1), 107; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12010107 - 13 Jan 2022

Cited by 2 | Viewed by 2200

Abstract

Presbycusis, physiological age-related hearing loss, is a major health problem because it is the most common cause of hearing impairment, and its impact will grow in the coming years with the aging population. Besides auditory consequences, the literature recently found an association between hearing loss and cognitive decline over the last two decades, emphasizing the importance of the early detection of presbycusis. However, the current hearing tests are not sufficient to detect presbycusis in some cases. Furthermore, the underlying mechanisms of this association are still under discussion, calling for a new field of research on that topic. In that context, this study investigates for the first time the interaction between presbycusis, eye movement latency and Stroop scores for a normal aging population. Hearing abilities, eye movement latency and the Stroop Victoria test were measured for 69 elderly (mean 66.7 ± 8.4) and 30 young (mean 25.3 ± 2.7) participants. The results indicated a significant relationship between saccade latency and speech audiometry in the silence score, independently from age. These promising results suggest common attentional mechanisms between speech processing and saccade latency. The results are discussed regarding the relationship between hearing and cognition, and regarding the perspective of expanding new tools for presbycusis diagnosis. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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11 pages, 1262 KiB

Open AccessArticle

Comparison of Visual Fixation Trajectories in Toddlers with Autism Spectrum Disorder and Typical Development: A Markov Chain Model

by Francesco Masedu, Roberto Vagnetti, Maria Chiara Pino, Marco Valenti and Monica Mazza

Brain Sci. 2022, 12(1), 10; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12010010 - 23 Dec 2021

Cited by 5 | Viewed by 2374

Abstract

Autism spectrum disorder (ASD) is a neurodevelopmental condition in which visual attention and visual search strategies are altered. Eye-tracking paradigms have been used to detect these changes. In our study, 18 toddlers with ASD and 18 toddlers with typical development (TD; age range 12–36 months) underwent an eye-tracking paradigm where a face was shown together with a series of objects. Eye gaze was coded according to three areas of interest (AOIs) indicating where the toddlers’ gaze was directed: ‘Face’, ‘Object’, and ‘No-stimulus fixation’. The fixation sequence for the ASD and TD groups was modelled with a Markov chain model, obtaining transition probabilities between AOIs. Our results indicate that the transition between AOIs could differentiate between toddlers with ASD or TD, highlighting different visual exploration patterns between the groups. The sequence of exploration is strictly conditioned based on previous fixations, among which ‘No-stimulus fixation’ has a critical role in differentiating the two groups. Furthermore, our analyses underline difficulties of individuals with ASD to engage in stimulus exploration. These results could improve clinical and interventional practice by considering this dimension among the evaluation process. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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11 pages, 925 KiB

Open AccessArticle

King-Devick Test Performance and Cognitive Dysfunction after Concussion: A Pilot Eye Movement Study

by Doria M. Gold, John-Ross Rizzo, Yuen Shan Christine Lee, Amanda Childs, Todd E. Hudson, John Martone, Yuka K. Matsuzawa, Felicia Fraser, Joseph H. Ricker, Weiwei Dai, Ivan Selesnick, Laura J. Balcer, Steven L. Galetta and Janet C. Rucker

Brain Sci. 2021, 11(12), 1571; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci11121571 - 27 Nov 2021

Cited by 2 | Viewed by 2716

Abstract

(1) Background: The King-Devick (KD) rapid number naming test is sensitive for concussion diagnosis, with increased test time from baseline as the outcome measure. Eye tracking during KD performance in concussed individuals shows an association between inter-saccadic interval (ISI) (the time between saccades) prolongation and prolonged testing time. This pilot study retrospectively assesses the relation between ISI prolongation during KD testing and cognitive performance in persistently-symptomatic individuals post-concussion. (2) Results: Fourteen participants (median age 34 years; 6 women) with prior neuropsychological assessment and KD testing with eye tracking were included. KD test times (72.6 ± 20.7 s) and median ISI (379.1 ± 199.1 msec) were prolonged compared to published normative values. Greater ISI prolongation was associated with lower scores for processing speed (WAIS-IV Coding, r = 0.72, p = 0.0017), attention/working memory (Trails Making A, r = −0.65, p = 0.006) (Digit Span Forward, r = 0.57, p = −0.017) (Digit Span Backward, r= −0.55, p = 0.021) (Digit Span Total, r = −0.74, p = 0.001), and executive function (Stroop Color Word Interference, r = −0.8, p = 0.0003). (3) Conclusions: This pilot study provides preliminary evidence suggesting that cognitive dysfunction may be associated with prolonged ISI and KD test times in concussion. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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Review

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19 pages, 295 KiB

Open AccessReview

Benefits of Implementing Eye-Movement Training in the Rehabilitation of Patients with Age-Related Macular Degeneration: A Review

by Anis Hilal, Mazen Bazarah and Zoï Kapoula

Brain Sci. 2022, 12(1), 36; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12010036 - 28 Dec 2021

Cited by 1 | Viewed by 1924

Abstract

Age-related macular degeneration (ARMD) is one of the most debilitating eye-related illnesses worldwide. Eye-movement training is evolving to be a non-invasive, rapid, and effective method that is positively impacting vision and QoL (quality of life) in patients suffering from ARMD. This review aims to highlight why a greater adoption of eye-movement training in the clinical and research setting is of importance. A PubMed and ResearchGate search was performed for articles published between 1982 and 2020. Patients with advanced ARMD tend to experience a diminished QoL. Studies regarding eye-movement training for patients with central vision loss revealed overall significant improvements in reading speeds, fixation, and saccade performance. They also experienced less fatigue. In select studies, eye-movement training revealed an improvement in binocular vision, fixation, reading speed, and diminished reading exhaustion. The process of eye-movement training used in some of the studies was rather empirical. The latter requires standardization so that a uniform and applicable methodology can be adopted overall. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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15 pages, 1583 KiB

Open AccessEditor’s ChoiceReview

The Organ of Vision and the Stomatognathic System—Review of Association Studies and Evidence-Based Discussion

by Grzegorz Zieliński, Zuzanna Filipiak, Michał Ginszt, Anna Matysik-Woźniak, Robert Rejdak and Piotr Gawda

Brain Sci. 2022, 12(1), 14; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci12010014 - 23 Dec 2021

Cited by 15 | Viewed by 4526

Abstract

The stomatognathic system is a functional complex of tissues and organs located within the oral and craniofacial cavities. The craniofacial anatomical factors and the biomechanics of the temporomandibular joints affect many systems throughout the body, including the organ of vision. However, few scientific reports have shown a relationship between the organ of vision and the stomatognathic system. The purpose of this review is to provide an overview of connections along neural, muscle-fascial, and biochemical pathways between the organ of vision and the stomatognathic system. Based on the literature presented in this review, the connections between the organ of vision and the stomatognathic system seem undeniable. Understanding the anatomical, physiological, and biochemical interrelationships may allow to explain the interactions between the mentioned systems. According to the current knowledge, it is not possible to indicate the main linking pathway; presumably, it may be a combination of several presented pathways. The awareness of this relationship among dentists, ophthalmologists, physiotherapists, and optometrists should increase for the better diagnosis and treatment of patients. Full article

(This article belongs to the Special Issue Eye Movements to Evaluate and Treat Attention Deficits)

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