Abstract
BACKGROUND
A better understanding of the relationship between eye movements required for reading and central visual field loss may facilitate the design of more effective personalized visual rehabilitation programs to improve access to information and quality of life.
OBJECTIVE
To determine the impact of central vision loss due to maculopathy on the oculomotor skills required for reading and tasks of varying complexity, eye-tracking technology was used.
METHODS
Case-control study. Participants were 17 cases (61.7 years (SD
RESULTS
Central vision loss due to maculopathy increases the number of fixations and saccadic movements, indicating more instability in and out of the region of interest. Visual search required more fixations (16.2
CONCLUSIONS
The results revealed the significant impact of central vision loss due to maculopathy on reading by increasing patterns of eye fixations, saccadic movements, and visual search strategies, as measured by eye-tracking technology. This technology may have high potential to improve the assessment and rehabilitation of people with maculopathy, and this may become key information for designing personalized interventions to improve the quality of life and autonomy of individuals with central vision loss.
1. Introduction
Central vision loss, characterized by vision impairment in the macular region, can be caused by various pathologies, and is one of the main causes of visual impairment in developed countries. This visual condition presents a significant challenge for the performance of daily tasks, especially those involving near vision, such as the recognition of fine details, faces, and the skills necessary for reading, with a substantial impact on the quality of life [1].
The ability to read is a fundamental skill in most daily tasks, communication, cognitive development, and learning. Ideal reading requires complex coordination of visual processes, including eye movements, which enables systematic and efficient exploration of texts. These movements primarily include eye fixations, saccadic movements, regressions, and visual searches [2, 3, 4].
Eye fixation involves the ability to hold one’s gaze in a specific position for a period. On the other hand, saccadic movements and regressions are rapid eye movements used to shift gaze from one point to another. Visual search is the process of scanning an area of interest to locate relevant information.
The macular area can alter eye movement planning, as evidenced by an increase in the number of fixations necessary to locate stimuli and instability in eye fixations [5, 6]. As a strategy to compensate for the difficulty of vision, some people resort to oculomotor strategies, even developing what is known as the preferential retinal locus (PRL).
Ocular motility training and visual rehabilitation can improve compromised oculomotor skills and visual task performance [7, 8]. Therefore, the measurement of visual ability should not be limited to parameters such as visual acuity and visual field, and it is essential to understand how people with central vision loss use their eyes to explore the environment.
Traditionally, ocular motility skills have been measured using techniques, such as microperimetry and scanning laser ophthalmoscopy [9, 10, 11, 12, 13, 14, 15, 16]. However, although these are gold standard assessment methods, the results they yield are monocular and generally quantify oculomotor skills on an individualized basis.
In this context, eye-tracking technology has been presented, consisting of devices with cameras or infrared light sensors that capture the position of the gaze. These innovative tools make it possible to record and analyze eye movement characteristics binocularly with precision and to evaluate behavior in various types of visual tasks.
A deeper understanding of the oculomotor behavior of this population is crucial for understanding the functional use of vision, facilitating the improvement and customization of visual rehabilitation programs, especially for reading, which is one of the most demanding tasks for people with central vision loss [17]. Furthermore, the application of this technology not only opens the door to the development of specialized tools but also makes it possible to obtain objective measurements in clinical settings and the effective evaluation of treatments and interventions, especially in terms of their performance against real-world visual tasks.
This study aimed to explore the impact of central vision loss on oculomotor skills required for reading and tasks of varying complexity using eye-tracking technology. This study aimed to provide a more comprehensive characterization of ocular motility in individuals with central vision loss and to propose a detailed analysis to identify possible patterns in visual scanning.
2. Materials and methods
A case-control study was conducted at the research laboratories of Complutense University of Madrid, Madrid, Spain. This research was reviewed by an independent ethical review board (Complutense University of Madrid Ethics Committee) and conformed to the principles and applicable guidelines for the protection of human subjects in biomedicine and was conducted in accordance with the principles of the Declaration of Helsinki. Written informed consent was obtained from all the participants prior to the start of the study.
Individuals with poor vision were recruited from the Macula-Retina Association. The inclusion criteria for this study were as follows: age
2.1. Eye tracking device and settings
Minimal reporting guidelines for research involving eye-tracking were followed [18]. Extended fixation, saccade, and visual search paradigms were chosen because they are useful for exploring the oculomotor system, visual fixation and saccade skills [19]. Stimuli were presented on an external 23-inch screen using the Tobii Pro Lab Screen-based edition [20]. A Tobii X2-60 device (60 Hz) (Tobii AB, Sweden) was used at a resolution of Full HD or 1080p. This eye tracker is able to record at 0.4∘ accuracy and 0.34∘ precision under good conditions of light and temperature. All stimuli were presented in white (RGB 240 240 240) on a black background (RGB 25 25 25) to ensure more than 80% contrast according to Weber’s formula.
2.1.1. Fixation task
The fixation test consisted of six central dots of different angular sizes (4.76∘, 3.81∘, 2.38∘, 1.90∘, 1.43∘, and 0.09∘). The dots were presented in the order of largest to smallest size for 10 s each. The test started with a central fixation cross and to avoid the visual afterimage effect; between each dot, a black screen was presented for 10 s, then a central cross appeared again for 1000 ms, and then the screen with the next central dot.
2.1.2. Saccades task
The test consisted of a dot with a size of 2.38∘dot. The test started with a central dot, which then appeared alternately to the left or right, returned to the center and then to the left or right again. The dot appeared 10 times in each position and had a duration of 2 s.
2.1.3. Visual search task
The test started with a fixation cross located at the center of the screen presented for 2 s. It consisted of 32 screens, including a stimulus of size 0.1∘. For this task, 32 c-shaped distractors and one target circle were presented. The location of the target and the direction of distractor C changed in each trial. The test was repeated twice for the 64 screens.
2.2. Eye-tracking test procedure
Under controlled conditions of room lighting (70–100 lux) (MAVO Monitor, Gossen, Germany) and temperature (24∘C) (TFA, Dostmann Wertheim, China), the test was carried out in a space free of distractors. Each participant was seated 60 cm from the screen, and a chinrest was used to reduce head movements.
Before initiating the test, the eye-tracker was calibrated for each subject, and a ad-hoc calibration consisting of a flashing black circle with two diagonal lines crossing in the center was performed. Before starting the calibration on the computer, the participant was provided with an explanation of the task via a printed stimulus. We used the resizing format, in which the flashing circle initially covered the entire screen for 5 s, allowing sufficient time for the subject to locate the center. Subsequently, the dot moved to one of the nine calibration positions, reaching a minimum size of 6∘ before changing position, and the dot returned to the center to facilitate the subject’s fixation. Maximal deviation is limited to
In the fixation test, the subject was instructed to look at a central dot of various angular sizes and hold the fixation steady for 10 s until the test was completed. In the saccade test, the subject was told that a white dot would appear in a central position, either to the left or to the right, and that they should look at it and keep their gaze on the dot until it disappears and the test is completed. In the visual search test, the subjects were instructed to find the circle and then press the space key as quickly as possible to continue with the next task. Each subject was video-recorded during the test.
2.3. Data and statistical analysis
The variables analyzed in the fixation task for each size presented were fixation stability, duration of fixations, number of fixations in the area of interest, number of saccades in the area of interest, total number of fixations, and total number of saccadic movements. Cronbach’s alpha was calculated to assess the internal consistency of the test. An alpha of 0.87 was obtained for the fixations test, 0.65 for the saccadic movements test and 0.87 for the visual search test. Fixation stability was calculated using the bivariate contour ellipse area (BCEA) formula at 68%:
where
In the saccadic movement test, several variables were analyzed, including the duration of fixations, the number of fixations, the time required to first direct the gaze to the area of interest, and the number, speed, amplitude and latency of saccadic movements. In the case of the visual search test, variables such as the time taken to locate the target, duration and number of fixations, and number, speed, amplitude and latency of saccadic movements were recorded. The direction of each saccadic movement was documented and classified as horizontal, vertical or oblique.
The data were standardized by calculating the logarithm of the decimal place for each. Descriptive statistics were expressed with mean and standard deviation values; for the comparison between groups, the t-student test, ANOVA with Bonferroni adjustment as required, as well as the Pearson test were used in the correlation studies between variables. Statistical significance was set at
3. Results
This study included 17 patients in (central vision loss group) and 17 controls. The central vision loss group comprised 12 women and 5 men with a mean age of 61.7 years (SD
The variables recorded for fixation, saccades, and visual search test results in each group are expressed as means and standard deviations (Tables 1, 2, and 3).
Fixation test results
Saccades test results
Visual search test results
Examples of experiments (1) fixation experiment. (2) saccades experiment. (3) visual search experiment.
Ellipse of ocular fixation positions. 1. Ellipse for stimulus size of 4.76∘. 2. Ellipse for stimulus size of 2.38∘. 3. Ellipse for stimulus size of 0.09∘.
Scan path of saccadic movements. 1. Scan path of saccades with direction from the center to the right of the persons with central vision loss. 2. Scan path of saccades with direction from the center to the right of the control group. Scan path of the saccadic movement of a person with central vision loss 4. Scan path of a person in the control group.
3.1. Fixation test
In the fixation test, people with central vision loss performed more fixations and saccadic movements in and out of the area of interest compared to the control group, which was observed for all six stimulus sizes presented (Table 3).
In the calculation of fixation stability (BCEA), for each of the six stimulus sizes, a significant difference (
3.2. Saccades test
In the saccadic movement test, for both the left and right directions, differences were found between cases and controls, with fixation duration, time to first glance, and saccade latency being worse in the central vision loss group. A disparity was observed in the time taken by individuals in both groups to perform saccadic movements depending on the direction of the movement. It was found that it took them longer to execute the saccadic movement to the left side in both groups (Table 3).
The test recordings were analyzed, and it was evident that people with central vision loss, in contrast to the control group, exhibited a nonlinear travel pattern. They performed a greater number of fixations and saccadic movements across space before reaching the target (Fig. 3).
3.3. Visual search test
In the visual search test, compared to controls, the central vision loss subjects needed more fixations (16.2
The direction of saccadic movements was examined, revealing that persons with central vision loss executed a greater number of movements in the oblique direction (6.7
4. Discussion
The aim of this study was to analyze the impact of loss of central vision on the ocular motility skills required for reading. For this purpose, a protocol was created to assess eye fixations, saccadic movements, and visual search measured using eye-tracking technology.
4.1. Fixation test
This assessment was carried out to explore fixation stability, which is considered a fundamental skill essential for reading. During the test, participants were asked to keep their gaze fixed or as steady as possible on a given point, however, it was observed that people with central vision loss exhibited a greater number of fixations and saccadic movements compared to the control group, in relation to the five stimulus sizes presented.
A statistically significant difference (
Fixation stability using the BCEA calculation indicates that the area of the ellipse calculated for individuals with central vision loss spans a considerably larger area than those in the control group, suggesting fixation instability, which is consistent with previous studies [12, 13, 15, 23]. This variation is intensified against the largest stimulus size (4.76∘) and the smallest stimuli (1.43∘ and 0.09∘). This pattern suggests the existence of an optimal stimulus size for each individual, underlining the influence that stimulus size may have on oculomotor behavior 24 and highlighting the potential advantage of an adequate magnification [24].
4.2. Saccades test
This test aimed to analyze oculomotor skills related to the transition of gaze from one area of interest to another, specifically to the left or right positions, which are necessary to move from one word to another during reading. A statistically significant difference was observed in the metrics of duration of fixations, time to first visualize the stimulus, and latency of saccadic movements, both in the left and right directions, which were worse in the group with central vision loss.
Previous studies related to saccadic movements have found, as in our study, an increase in the duration and number of fixations as well as in the speed and amplitude of saccadic movements, finding a behavior where the higher the speed, the greater the amplitude of saccadic movements, and analyzing that these elevated results in the metrics correlate positively with the size of the scotoma [25, 26, 27].
In relation to the time to find the target and the latency of saccades, people with central vision loss require a significantly longer time to see the target for the first time than healthy people. Even comparative studies with other pathologies that restrict the visual field show that people with macular degeneration and retinitis pigmentosa require more time to perform saccadic movements and find the stimulus [27].
On the other hand, when examining the test recordings, it was observed that individuals in the control group executed a direct saccadic movement toward the target, while those with central vision loss presented a nonlinear trajectory, adopting a curved upward or downward shape before reaching the target, which required them to perform multiple fixations and saccades. This behavioral pattern has been identified in previous research and is defined as saccade tortuosity, indicating that these deviations in movement are usually directed toward the scotoma [28, 29, 30].
Regarding direction, disparities are identified in the group of people with central vision loss, as they need to perform a greater number of fixations, make more saccadic movements, and spend more time locating the target when presented on the left side. This observation could provide clues about the position of the person’s scotoma, but it could also be justified that the usual direction of reading is from left to right, and people may be more familiar with that movement [31].
4.3. Visual search test
The purpose of this test is to assess the ability of individuals to identify a specific visual stimulus in the presence of distractions. This task increased complexity compared to previous activities and is fundamental in the reading process, as it is involved in locating line beginnings, words, line changes, and general visual scanning of texts.
In this case, as in previous studies, significant differences were found between groups in most of the metrics analyzed, indicating difficulty in visual search tasks in people with central vision loss [8, 32]. This can occur because of the lack of a specific scanning pattern, and it is also indicated that the person may try to avoid the scotoma or even be unaware of its presence, as in negative scotomas, where the brain compensates for or fills in the missing information [28, 30, 33].
As for the time to perform visual search tasks, people in the central vision loss group required much more time than those in the study group, which was confirmed by previous research [5, 34]. Several theories have been proposed to explain these results. First, it is suggested that the difficulty in perceiving information in the central region could lead people to repeatedly scan the area of interest and scanning each section until the target is identified. This phenomenon is more pronounced in the absence of defined search patterns. Second, the signal detection theory exists. According to this theory, due to a decrease in change detection ability, people with central vision loss may show prolonged (longer) attention to the area of interest to compensate for the loss of visual acuity [5, 35].
The third argument is that unlike reading, where movement is usually horizontal, in visual search tasks, movements can be in different directions; therefore, more time is required to find a target [36]. All three explanations could help understand why people with central vision loss perform more oblique movements than horizontal or vertical movements in visual search tasks.
In our investigation, a significantly higher number of eye fixations and saccadic movements were observed in the central vision loss group. This high visual activity could be due, in part, to the possibility that the information initially presented was not accurate for the individual. Consequently, the individual performs more eye movements to integrate the information that manages to enter his visual field. This phenomenon has been found in other studies and is directly linked to a prolongation of the duration of fixations as well as to a longer latency in the execution of saccadic movements [5, 28, 35].
Regarding the amplitude of saccadic movements, in our study, it was found to be the only metric with lower results than the control group; similar results have been found in previous research [5, 37, 38]. In visual search tasks, several stimuli are usually presented in a delimited area, which implies that the person must reduce their search routes to scan and discriminate between distractors and stimuli. This could explain the reduction in the amplitude of the saccades, especially if there is a restriction of the visual field.
4.4. Impact on reading
Reading requires the eyes to perform a series of eye movements such as saccadic movements, regressions, fixations, and visual search skills [25]. If there is any inaccuracy in these skills, reading process and comprehension may be impaired.
Based on our results, oculomotor challenges were found in individuals with central vision loss, which could affect reading. These difficulties may cause fixation instability and altered saccadic movements, where some parts of the words are omitted, which could lead to a higher number of regressions and complicate the search for the next line [21, 39].
There is evidence for the importance of oculomotor training in improving visual skills and reading performance in subjects with central vision loss [21]. For them, the binocular evaluation of the person is considered important in order to understand the visual functioning of this person [40]. Eye-tracking devices can provide information on binocular ocular motility behavior. This information may be useful for intervention decision making and for determining better visual rehabilitation strategies [21].
The main limitations of our study were the variability in the etiology of central vision loss and the lack of analysis of the scotomas of each individual. However, the low frequency of image capture of the eye-tracking device used and the difficulties during calibration implied the exclusion of part of the sample; therefore, the sample size is also an important limitation.
These limitations open the door to future research in which results can be compared with reading assessments and oculomotor behavior can be measured with eye-tracking devices during reading tasks. It is important to consider the relationship between scotoma size and time to central vision loss. Further research with a larger number of participants and different tasks is required to confirm these findings.
5. Conclusions
The results obtained suggest that there is an impact of central vision loss on the ocular motility skills necessary for reading, manifesting as fixation instability, difficulty in performing saccadic movements, and the lack of specific visual search patterns. This usually translates into a greater number and duration of fixations and saccadic movements and a longer time to complete visual tasks, which can affect a person’s performance in near vision tasks such as reading. Assessments using eye-tracking technology could provide a more detailed analysis of the difficulties faced by people with central vision loss. The results obtained yielded relevant knowledge about the visual functioning of individuals beyond visual acuity and may become an important resource for the design of personalized interventions to improve the quality of life and autonomy of people with central vision loss.
Funding
No funding was received from funding agencies in the public, commercial, or nonprofit sectors.
Author contributions
CONCEPTION: L.G-V, P.C, J.A.G-P, J.L.H-V.
PERFORMANCE OF WORK: L.G-V, P.C, J.L.H-V.
INTERPRETATION OR ANALYSIS OF DATA: L.G-V, P.C, J.L.H-V.
PREPARATION OF THE MANUSCRIPT: L.G-V, P.C, J.L.H-V.
REVISION FOR IMPORTANT INTELLECTUAL CONTENT: L.G-V, P.C, J.A.G-P, J.L.H-V.
SUPERVISION: P.C, J.L.H-V.
Ethical considerations
The study was approved by the Ethics Committee of the Universidad Complutense de Madrid (No. CE_20221215-10_SOC). All subjects read and signed an informed consent form before participating in the study. The study was conducted in accordance with the principles of the Declaration of Helsinki.
Footnotes
Acknowledgments
The authors acknowledge the University of Costa Rica for financial support provided to Leonela González Vides in her academic training abroad as a fellow under the Academic Mobility program of the Office of International Affairs and External Cooperation.
Conflict of interest
The authors have no conflicts of interest to report.
