Abstract
Background
Reading difficulties are commonly reported in Parkinson's disease (PD). So far, only a few studies have assessed reading in PD, most of them confirming a different pattern in patients compared with healthy populations. Impaired oculomotor control is an early feature of PD. Cognitive deficits, on the other hand, may appear early, but they are most prominent at later stages. Although these two factors are thought to be responsible for the alterations in reading performance, it is unclear how each factor contributes to them.
Objectives
To evaluate eye movements during reading in PD and healthy controls (HCs).
Methods
Data from 42 HCs (36% men) and 48 patients with PD (67% men) at Hoehn and Yahr stages ≤3 were analyzed. PD participants were further divided into 2 groups based on their Montreal Cognitive Assessment (MoCA) score using a cutoff of ≥26. Eye movements were recorded with Tobii Pro Spectrum, a screen‐based eye tracker with a sampling rate of 1200 Hz.
Results
PD participants performed fewer fixations per second (P = 0.033), with a longer mean (P = 0.037) and standard deviation fixation duration (P = 0.033) than HC, and further analysis showed that only patients with a lower MoCA score performed worse than HCs. Reading parameters were weakly associated with MoCA scores, irrespective of age and education.
Conclusion
Changes in the reading pattern of PD patients are probably attributed to cognitive rather than pure oculomotor alterations.
Keywords: Reading, Parkinson's Disease, Cognition, Eye‐movements, Fixation duration
Reading is a complex task that involves visual and cognitive processes. Saccades bring the fovea, where visual acuity is optimal, to words of interest, although information from the periphery influences the reading process as well. Words are then fixated in order to be interpreted. Fixation duration is determined by various factors, such as linguistic properties of the text as well as the reader's mental and cognitive status. 1 , 2 Hence, fixation position and saccade amplitude are measures of space that describe the direction and sequence of processing, whereas fixation duration represents a temporal measure and indicates processing load. 3 Normally, there is a choice of words that are fixated and some that are skipped during reading. The first are content words and are usually larger in size, whereas those that are omitted are functional words that are smaller, and although not fixated they are still important, and they are processed during reading, seen parafoveally. 1 Not all saccades during reading are progressive, moving the eyes forward to the next word or within the same word. Of the saccadic eye movements during reading, 10% to 15% are regressive, toward previous words, in order to acquire missing information, or within the same word in order to correct a progressive saccade that was too long. 1
Brain structures that are involved in natural reading and correlate to fixation duration have been identified in functional magnetic resonance imaging (fMRI) studies, and they include cortical areas that are associated with attention, language processing, and oculomotor control as well as striate and peristriate regions. 2 Variations in eye movement patterns during reading and other tasks are to some extent attributed to individual differences in working memory. 4
Parkinson's disease (PD) is characterized by motor symptoms such as hypokinesia and bradykinesia, rigidity, tremor, and postural instability as well as a variety of nonmotor symptoms, such as oculomotor and reading difficulties. The best described oculomotor alterations in PD are increased saccadic latency, reduced frequency and amplitude of voluntary gaze shifts, and reduced gain in smooth pursuit eye movements. 5 Typically, hypokinesia is reflected in the low amplitude of saccadic eye movements. 6 Previous research has indicated that slower reading in PD is caused by a higher number of regressive saccades and longer fixation duration compared with those of healthy controls (HCs) probably attributed to cognitive deficits, 7 , 8 but literature on the topic is restricted. A recent publication revealed that the differences in reading between PD and HCs are mainly attributed to cognitive deficits that may occur in PD, whereas the reading pattern does not differ significantly between cognitively intact PD patients and HCs. 9
The project aims to examine the differences in reading patterns between PD and HCs and the role of cognition.
Methods
Participants
A total of 50 PD patients of unilateral to mild to moderate disease (Hoehn and Yahr stages 1–3, Schwab and England scores 70%–90%) and 43 HCs were recruited at the Center of Neurology, Academic Specialist Centrum, Stockholm, Sweden. The diagnosis was based on the International Parkinson and Movement Disorder Society Clinical Diagnostic Criteria for PD. 10 The study was approved by the Stockholm Ethical Committee diarienummer (DNR): 2018/437–31/2), and participants provided written and oral informed consent according to the Declaration of Helsinki. Individuals suffering from eye conditions such as macular degeneration or nonoperable/noncorrected cataract were excluded, and vision was normal or corrected to normal (visual acuity of a Logarithm of the Minimum Angle of Resolution (logMAR) score ≤0.00), regarding both refraction and presbyopia. Because of poor data quality, 1 HC and 2 PD participants were excluded from the analysis, which left 42 HCs (36% men) and 48 PD participants (67% men).
The participants were clinically assessed with the Unified Parkinson's Disease Rating Scale (UPDRS). 11 Cognition was assessed with the Montreal Cognitive Assessment (MoCA). 12
Apparatus and Stimuli Presentation
Tobii (Stockholm, Sweden) Pro Spectrum, a screen‐based eye tracker with a sampling rate of 1200 Hz, was used for the binocular recording eye movements. Stimuli were presented on the native 23.8″ Tobii Pro Spectrum screen (EIZO [Ishikawa, Japan] FlexScan EV2451) with a pixel resolution 1920 × 1080 (52.8 × 29.7 cm). The screen was located approximately 65 cm in front of the participant, who was sitting on a steady and comfortable chair in a dimly lit room. The Landolt C Chart was used to assess visual acuity, and participants were included only if they received a logMAR score ≤0.00 after correcting for refraction and/or presbyopia. Participants silently read a Swedish text written in black and taken from the international reading texts 13 that was displayed on a bright white screen. PD patients were assessed in on medication status. A 5‐point calibration followed by 4 points of validation was performed on each participant before the first trial. Recalibrations were made if deemed necessary by the examiner.
Data Processing
The recorded data were filtered through the Tobii Identification by Velocity Threshold algorithm that identifies fixations and saccades in the raw gaze data based on a velocity criterion. A default value of 30°/s for the velocity threshold was used for the detection of saccades. Gaze parameters were based on left and right eye averages, but when only 1 eye was found for a data sample, that eye was used in the computation.
During the reading task, the total recording time (seconds), words per minute, fixation duration (milliseconds), and number of fixations per second as well as the proportion of progressive and regressive saccades computed as the percentage of regressive (leftward and/or upward) saccades among all saccades (regression frequency) were measured. Saccadic amplitude (both absolute and Euclidian distance between the start and end positions in the horizontal/vertical axis in degrees of visual angle) was also measured. Fixation dispersion (the standard deviation [SD] of the [average] horizontal/vertical fixation position in degrees of visual angle), the ratio of the number of detected fixation events to the number of detected saccade events, and last pupil size (millimeters) were also computed.
Statistical Analysis
Statistical analysis was done with IBM (Armonk, NY) SPSS 25 Statistic Data Editor, and the level of 0.05 was considered significant. The Mann–Whitney nonparametric test was used for comparisons between 2 groups, Kruskal–Wallis was used for comparisons between more than 2 groups, and pairwise comparisons using the Bonferroni correction for multiple tests was applied. Chi‐square was used to compare ratios between groups. The cutoff score of 26 in MoCA was used to identify the effect of cognition on reading parameters. 12 , 14
Results
The clinical and demographical characteristics of the participants are summarized in Table 1. Our groups (HC vs. PD) did not differ in age and years of education, whereas the proportion of women was higher in the HC group than in the PD group (P = 0.006). Regarding cognition, the groups scored similarly in MoCA; however, there was a statistically significant difference in the scores of the visuospatial/executive domain, with HCs scoring higher than PD participants (P = 0.002).
TABLE 1.
Demographic and clinical characteristics of PD patients versus HC participants
| Demographics | HCs, n = 42 | PD Patients, n = 48 | P |
|---|---|---|---|
| Age, years | 62.5 (16.25) | 64.5 (11.5) | 0.6 |
| Education, years | 15 (4.25) | 16 (4) | 0.7 |
| Sex, female/male | 27/15 | 16/32 | 0.006 |
| Years since diagnosis | 2.5 (3.5) | NA | |
| LEDD | 545 (496.25) | NA | |
| UPDRS total | 36.5 (21.25) | NA | |
| Schwab and England | 90 (10) | NA | |
| MoCA | 27 (3) | 27 (3) | 0.1 |
| MoCA ≥26, yes/no | 34/8 | 32/16 | 0.16 |
| Visuospatial/executive | 5 (1) | 4 (2) | 0.002 |
Values are reported as medians and interquartile ranges in parentheses, except for sex, ethnicity, and grouping based on MoCA score, which are reported as absolute numbers.
Abbreviations: PD, Parkinson's disease; HCs, healthy controls; LEDD, levodopa equivalent daily dose; NA, not applicable; UPDRS, Unified Parkinson's Disease Rating Scale; MoCA, Montreal Cognitive Assessment.
Comparisons of the eye movement parameters during reading between the 2 groups, summarized in Table 2, revealed that PD participants performed fewer fixations per second (P = 0.033), with a longer mean and SD fixation duration (P = 0.037 and 0.033, respectively) than HCs. Other than that, no statistically significant differences could be identified.
TABLE 2.
Eye movement parameters during reading in the HC and PD groups
| Eye movement parameters | HCs, n = 42 | PD Patients, n = 48 | P |
|---|---|---|---|
| Total duration | 36.91 (11.63) | 38.9 (13.92) | 0.3 |
| Words/min | 237.36 (70.6) | 225.17 (71.66) | 0.3 |
| Fixations/s | 3.55 (0.87) | 3.38 (0.75) | 0.033 |
| Regression frequency | 20.89 (10.85) | 24.67 (14.58) | 0.2 |
| Fixation duration mean | 223.39 (46.88) | 249.23 (42.73) | 0.037 |
| Fixation duration SD | 102.09 (47.04) | 121.78 (60.54) | 0.033 |
| Fixation dispersion horizontal mean | 0.16 (0.2) | 0.2 (0.15) | 0.8 |
| Fixation dispersion horizontal SD | 0.14 (0.33) | 0.14 (0.29) | 0.5 |
| Fixation dispersion vertical mean | 0.12 (0.11) | 0.12 (0.2) | 0.3 |
| Fixation dispersion vertical SD | 0.11 (0.15) | 0.11 (0.18) | 0.7 |
| Saccade distance horizontal mean | 3.26 (0.89) | 3.05 (1.51) | 0.2 |
| Saccade distance horizontal SD | 3.4 (0.74) | 3.2 (0.71) | 0.2 |
| Saccade distance vertical mean | 0.77 (0.48) | 0.79 (0.58) | 0.4 |
| Saccade distance vertical SD | 1.8 (1.43) | 1.77 (1.35) | 0.1 |
| Euclidean saccade distance mean | 3.74 (0.76) | 3.36 (1.26) | 0.07 |
| Euclidean saccade distance SD | 3.64 (1.32) | 3.57 (1.14) | 0.1 |
| Pupil diameter mean | 2.6 (0.45) | 2.53 (0.39) | 0.09 |
| Pupil diameter SD | 0.12 (0.06) | 0.13 (0.07) | 0.5 |
| Fixation/saccades ratio | 0.79 (0.33) | 0.72 (0.46) | 0.4 |
Values are reported as medians and interquartile ranges. Total duration is reported in seconds. Regression frequency: percentage of regressive (leftward and/or upward) saccades among all saccades. Fixation duration is reported in milliseconds. Fixation dispersion for a single fixation event: the SD of the (average) horizontal/vertical fixation position reported in degrees of visual angle. Saccade distance (absolute and Euclidean) is reported in degrees of visual angle, and pupil diameter is reported in millimeters. Statistically significant differences (P < 0.05) are bold.
Abbreviations: HCs, healthy controls; PD, Parkinson's disease; SD, standard deviation.
Based on our hypothesis that cognition might play an important role in reading performance, we examined whether dividing the PD group into 2 subgroups based on MoCA score would provide further information. Given that a MoCA score ≥26 is considered normal, in the PD group we identified 2 subpopulations: 1 consisted of 32 participants with a MoCA score ≥26, and 1 consisted of 16 participants with a MoCA score <26. Results of the comparisons between the PD groups are summarized in Table 3, whereas comparisons between the reading parameters of all 3 groups (HC, PD MoCA ≥26, PD MoCA <26) are summarized in Table 4. The main finding was that the mean (P = 0.011) fixation duration differs between HCs and the cognitively affected PD group, whereas the difference between HCs and the cognitively intact PD group is not significant. In addition, the nonsignificant differences between the groups in total duration, words per minute, and fixations per second, especially between the HC and PD MoCA <26 groups (P = 0.06, 0.06, and 0.07, respectively) indicate a trend toward a worse performance in the latter.
TABLE 3.
Demographic and clinical characteristics of PD MoCA ≥26 versus PD MoCA <26 participants
| Clinical parameters | PD MoCA ≥26, n = 32 | PD MoCA <26, n = 16 | P |
|---|---|---|---|
| Age, years | 65.5 (14.25) | 64 (8.25) | 0.4 |
| LEDD | 540 (503.75) | 600 (526.25) | 0.6 |
| UPDRS Part 1 | 1 (2) | 1.5 (1) | 0.96 |
| UPDRS Part 2 | 10 (5.5) | 9.5 (6.75) | 0.7 |
| UPDRS Part 3 | 19 (16.5) | 24.5 (16.5) | 0.6 |
| UPDRS Part 4 | 2 (5.25) | 2 (2.75) | 0.96 |
| UPDRS total | 36 (17.25) | 41.5 (30.25) | 0.6 |
| Years since diagnosis | 2.5 (3.75) | 2.5 (3.5) | 0.8 |
| Schwab and England | 90 (10) | 90 (10) | 0.9 |
Values are reported as medians and interquartile ranges.
Abbreviations: PD, Parkinson's disease; MoCA, Montreal Cognitive Assessment; LEDD, levodopa equivalent daily dose; UPDRS, Unified Parkinson's Disease Rating Scale.
TABLE 4.
Eye movement parameters during reading in HCs, PD MoCA ≥26, and PD MoCA <26
| Eye movement parameters | HCs, n = 42 | PD MoCA ≥26, n = 32 | PD MoCA <26, n = 16 | P | Multiple Comparisons Bonferroni |
|---|---|---|---|---|---|
| Total duration | 36.91 (11.63) | 37.94 (10.25) | 43.32 (25.51) | 0.06 | |
| Words/min | 237.36 (70.6) | 230.88 (59.37) | 202.22 (93.45) | 0.06 | |
| Fixations/s | 3.54 (0.87) | 3.41 (0.74) | 3.25 (0.82) | 0.07 | |
| Regression frequency | 20.89 (10.85) | 23.92 (13.05) | 26.95 (14.82) | 0.1 | |
| Fixation duration mean | 223.39 (46.88) | 237.69 (46.22) | 269.49 (84.01) | 0.015 | HCs–PD MoCA <26 = 0.011 |
| Fixation duration SD | 102.09 (47.04) | 111.24 (53.17) | 146.54 (82.17) | 0.04 |
HCs–MoCA <26 = 0.03 PD MoCA ≥26–MoCA <26 = 0.03 |
| Fixation dispersion horizontal mean | 0.16 (0.2) | 0.15 (0.14) | 0.26 (0.36) | 0.06 | |
| Fixation dispersion horizontal SD | 0.14 (0.33) | 0.1 (0.18) | 0.3 (0.8) | 0.026 | PD MoCA ≥26–MoCA <26 = 0.028 |
| Fixation dispersion vertical mean | 0.12 (0.11) | 0.11 (0.2) | 0.15 (0.21) | 0.4 | |
| Fixation dispersion vertical SD | 0.11 (0.15) | 0.09 (0.22) | 0.16 (0.16) | 0.2 | |
| Saccade distance horizontal mean | 3.26 (0.89) | 3.03 (1.39) | 3.23 (2.11) | 0.4 | |
| Saccade distance horizontal SD | 3.4 (0.74) | 3.19 (0.55) | 3.37 (1.9) | 0.2 | |
| Saccade distance vertical mean | 0.77 (0.48) | 0.86 (0.72) | 0.64 (0.54) | 0.5 | |
| Saccade distance vertical SD | 1.8 (1.43) | 1.9 (1.51) | 1.43 (0.54) | 0.2 | |
| Euclidean saccade distance mean | 3.74 (0.76) | 3.3 (1) | 3.54 (2.02) | 0.2 | |
| Euclidean saccade distance SD | 3.64 (1.32) | 3.57 (0.71) | 3.62 (1.84) | 0.2 | |
| Pupil diameter mean | 2.6 (0.45) | 2.43 (0.42) | 2.64 (0.22) | 0.05 | |
| Pupil diameter SD | 0.12 (0.06) | 0.13 (0.08) | 0.12 (0.05) | 0.8 | |
| Fixation/saccades ratio | 0.79 (0.33) | 0.76 (0.52) | 0.63 (0.43) | 0.5 |
Values are reported as medians and interquartile ranges. Total duration is reported in seconds. Regression frequency: percentage of regressive (leftward and/or upward) saccades among all saccades. Fixation duration is reported in milliseconds. Fixation dispersion for a single fixation event: the SD of the (average) horizontal/vertical fixation position reported in degrees of visual angle. Saccade distance (absolute and Euclidean) is reported in degrees of visual angle, and pupil diameter is reported in millimeters. Statistically significant differences (P < 0.05) between pairs of groups are bold.
Abbreviations: HCs, healthy controls; PD, Parkinson's disease; MoCA, Montreal Cognitive Assessment; SD, standard deviation.
Correlation analysis revealed weak but significant association between MoCA scores and total duration (r = −0.232, P = 0.028), words per minute (r = 0.266, P = 0.011), and mean and SD of fixation duration (r = −0.268 [P = 0.011] and r = −0.284 [P = 0.007], respectively). The correlations remained significant after controlling for age, sex, and education. In addition, MoCA correlated with the motor subscore of the UPDRS Part 3 (r = −0.21, P = 0.047), and the score of the UPDRS Part 3 correlated with fixations per second and mean and SD of fixation duration (r = −0.264 [P = 0.012], r = 0.227 [P = 0.032], and r = 0.273 [P = 0.009], respectively). However, the motor score of the UPDRS did not differ significantly between the 2 PD subpopulations (Table 3).
Our population consisted of more male than female participants in the PD subgroup than in the HC subgroup (P = 0.006). To explore if this difference influenced our results, we conducted separate comparisons within the male and female groups. We found that in the female group, the total duration (P = 0.058), words per minute (P = 0.058), fixation duration mean (P = 0.334) and SD (P = 0.07), and fixations per second (P = 0.318) did not differ significantly between the HC, PD MoCA ≥26, and PD MoCA <26 subgroups. In the male group, however, these parameters differed significantly between the 3 subgroups (P = 0.047, P = 0.047, P = 0.039, P = 0.023, and P = 0.024, respectively).
Discussion
During our study, we were able to identify differences in reading patterns between PD patients and HCs. Interestingly, though, the differences seem to become more obvious between PD patients who are cognitively affected and HCs, and this was further supported by the association between the MoCA score and the eye movement parameters. Of all the reading parameters, it was fixation duration that was prolonged in PD, whereas regression frequency did not differ significantly between the groups. This is in accordance with our group's previous findings, 7 where fixation duration was significantly longer in PD, especially when cognition was impaired, compared with HCs. However, we did not manage to identify statistically significant differences in the regression frequency between our groups despite a trend toward more regressive saccades in the cognitively affected PD patients (HC < PD cognitively normal < PD cognitive affected). Similarly, differences in total duration and number of words per minute did not reach statistical significance (P = 0.06 in both cases), but it would be reasonable to assume that cognitively intact PD patients performed almost similar to HCs, whereas the cognitively affected PD group read slower. The fact that the motor score of the PD groups was similar is indicative of a rather cognitive than motor effect on reading performance.
A separate analysis revealed that differences in the reading parameters were more profound between the male participants of different subgroups (HCs, PD MoCA ≥26, PD MoCA <26), whereas differences between the female subgroups did not reach statistical significance despite a trend toward a worse performance in the MoCA <26 group. Although research that examines reading performance in males and females has mainly focused on younger populations, 15 , 16 in an educational context, results are inconclusive, pointing toward a female predominance in reading performance. Our results should be examined with caution, as they do not clearly confirm such a conclusion.
While the eyes fixate on a word, cognitive processes take place for new information to be acquired. 1 Longer fixation duration during reading could be related to deficits in decision‐making processes, attention, and working memory, which are known to be affected in PD, thus reflecting the cognitive load that prolongs word processing. 17 Moreover, sentence comprehension is impaired in PD, probably as a result of deficits in working memory. 18 Interestingly, it has been shown that reading in Alzheimer's disease is slower as a result of longer fixation durations and short saccadic amplitudes while the eyes move to the next word as well as a higher number of regressions both to the previous words and within the same word. 19 However, our study failed to indicate differences in saccadic amplitudes between groups.
Studies that compared reading and pseudo‐reading (sequential scanning task) in healthy individuals revealed a common core eye movement control brain network similar to that of sequential scanning tasks and single‐saccade movements. 2 , 20 In addition, they showed increased activation of the language network and the lateral frontal eye fields (FEFs) during natural reading while brain regions related to attention were activated in pseudo‐reading. These findings indicate that eye movements during natural reading present with a more reflexive character of the saccades and greater fixational control as well as a higher automatic phonological processing, requiring less attentional resources, compared with sequential scanning. The reflexive character of the saccades during reading resembles that of visually guided saccades, visual input coming from the nearby words as perceived by parafoveal areas. Although the FEFs are involved in fixation initiation, the supplementary eye fields (SEF) activation has been shown to correlate with fixation duration, probably indicating that the SEF are responsible for the integration of eye movement control with the cognitive processes required during reading. 2 Both SEF and FEF hypoactivity during voluntary saccadic tasks has been described in fMRI recordings of PD patients. 21 Similarly, metabolic changes in the frontal lobes of cognitively impaired PD patients have recently been described using proton magnetic resonance spectroscopy. 22 Another study indicated higher activity in the frontal and parietal cortices of young‐onset PD patients with the use of fMRI, possibly compensating for abnormalities in saccadic and cognitive functions. 23
Studies on number reading have shown contradictory results, with 1 study showing that PD affects only word reading and not number reading, 8 whereas another showed that saccadic reading assessed with number reading instead of words is impaired in PD even when the semantic context is absent. 24 A study on reading performance in PD with the use of the Alouette test has also shown that PD patients read fewer words per minute. 25 The Alouette test comprises common words put together in a way that lacks meaning and therefore reduces predictability related to the reader's previous experience. These findings indicate that language and sentence comprehension alone cannot entirely explain the differences in reading performance between PD patients and HCs.
Our study is not without limitations. First, we only used MoCA for the characterization of cognition of our participants. Despite the fact that MoCA is 1 of the most popular and well‐accepted screening tools for cognition in PD, it is not enough to support a diagnosis of mild cognitive impairment or dementia without a more thorough evaluation. A low MoCA score is, however, an indicator of affected cognition commonly used in the everyday practice. Second, methodologically we used an approach that was based on visual perception and motor control, not taking into account the linguistic properties of the text. That said, we have not examined the differences in gaze duration, which compared with fixation duration computes the sum of all fixation durations within the same word. Similarly, we have not differentiated content words from function words to compare PD and HC eye behavior while reading words of various contextual gravity. In addition, we have not compared the number of progressive interword (between) and intraword (within the same word) saccades between HCs and PD patients. Last, although prolonged saccadic latency is a common feature in PD, probably reflecting difficulties in working memory and executive function, we have not identified whether this could contribute to slower reading in PD.
In conclusion, our study is 1 of the few that assess reading in PD. The main findings indicate that PD patients perform longer fixations while reading, leading to slower reading, presumably as a result of cognitive rather than oculomotor impairment. Further studies combining visual processing and oculomotor control with a more psycholinguistic approach, together with imaging techniques, in cognitively well‐characterized patients would add to our knowledge on the subject.
Author Roles
(1) Research Project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript Preparation: A. Writing of the First Draft, B. Review and Critique; (4) Responsible for the Integrity of the Data and the Accuracy of the Data Analysis.
P.T.: 1A, 1B, 1C, 2A, 2B, 2C, 3A, 3B, 3C, 4
M.N.: 1A, 1B, 1C, 2C, 3B
G.Ö.S.: 1A, 1B, 3B
O.L.: 1A, 1B, 3B
P.S.: 1A, 1B, 3C
I.M.: 1A, 1B, 1C, 2A, 2B, 2C, 3A, 3B
Disclosures
Ethical Compliance Statement: The study was approved by the Stockholm Ethical Committee (Diarienummer: 2018/437–31/2). All participants provided written and oral informed consent according to the Declaration of Helsinki. Written consent forms are archived at the Center of Neurology, Academic Specialist Centrum, Stockholm, Sweden. All authors confirm that they have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.
Funding Sources and Conflicts of Interest: The study was supported by Vinnova, Sweden's innovation agency (Grant 2017–02317; “Early Detection of Alzheimer's and Parkinson's Disease Based on Eye‐Tracking and AI”). M. Nilsson and G. Ö. Seimyr own equity in Optolexia, a company whose aim is to offer new technologies for the assessment of reading skill based on eye tracking and artificial intelligence. The venture is a result of projects funded by Sweden's innovation agency—Vinnova—(2014–03459, 2017–02317) and Karolinska Institutet Innovations.
Financial Disclosures for the Previous 12 Months: P.S. receives funding from Vinnova, the Parkinson Research Foundation, the Stockholm County Council, and the Wallenberg Clinical Scholarship as well as honoraria from AbbVie. I.M. receives funding from the Stockholm County Council (FoUI‐960,041) and the Parkinson Research Foundation, Stockholm. The authors declare that there are no additional disclosures to report.
Acknowledgments
We express thanks to Vinnova and to the Sigvard and Marianne Bernadotte Research Foundation for Children's Eye Care.
References
- 1. Rayner K. Eye movements in reading and information processing: 20 years of research. Psychol Bull 1998;124(3):372–422. [DOI] [PubMed] [Google Scholar]
- 2. Henderson JM, Choi W, Luke SG, Desai RH. Neural correlates of fixation duration in natural reading: Evidence from fixation‐related fMRI. Neuroimage 2015;119:390–397. [DOI] [PubMed] [Google Scholar]
- 3. Radach R, Kennedy A. Theoretical perspectives on eye movements in reading: Past controversies, current issues, and an agenda for future research. Eur J Cogn Psychol 2004;16(1–2):3–26. [Google Scholar]
- 4. Luke SG, Darowski ES, Gale SD. Predicting eye‐movement characteristics across multiple tasks from working memory and executive control. Mem Cognit 2018;46(5):826–839. [DOI] [PubMed] [Google Scholar]
- 5. Pinkhardt EH, Kassubek J. Ocular motor abnormalities in parkinsonian syndromes. Parkinsonism Relat Disord 2011;17(4):223–230. [DOI] [PubMed] [Google Scholar]
- 6. Macaskill MR, Graham CF, Pitcher TL, Myall DJ, Livingston L, van Stockum S, et al. The influence of motor and cognitive impairment upon visually‐guided saccades in Parkinson's disease. Neuropsychologia 2012;50(14):3338–3347. [DOI] [PubMed] [Google Scholar]
- 7. Waldthaler J, Tsitsi P, Seimyr G, Benfatto MN, Svenningsson P. Eye movements during reading in Parkinson's disease: A pilot study. Mov Disord 2018;33(10):1661–1662. [DOI] [PubMed] [Google Scholar]
- 8. Yu CY, Lee T, Shariati MA, Santini V, Poston K, Liao YJ. Abnormal eye movement behavior during reading in Parkinson's disease. Parkinsonism Relat Disord 2016;32:130–132. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Stock L, Krüger‐Zechlin C, Deeb Z, Timmermann L, Waldthaler J. Natural Reading in Parkinson's disease with and without mild cognitive impairment. Front Aging Neurosci 2020;12:120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Postuma RB, Berg D, Stern M, et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 2015;30(12):1591–1601. [DOI] [PubMed] [Google Scholar]
- 11. Fahn S, Elton RL. UPDRS program members. Unified Parkinsons disease rating scale. In: Fahn S, Marsden CD, Goldstein M, Calne DB, eds. Recent Developments in Parkinsons Disease. Vol 2. Florham Park, NJ: Macmillan Healthcare Information; 1987:153–163. [Google Scholar]
- 12. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005;53(4):695–699. [DOI] [PubMed] [Google Scholar]
- 13. Trauzettel‐Klosinski S, Dietz K. Standardized assessment of Reading performance: The new international Reading speed texts IReST. Invest Ophthalmol Vis Sci 2012;53(9):5452–5461. [DOI] [PubMed] [Google Scholar]
- 14. Dalrymple‐Alford JC, MacAskill MR, Nakas CT, Livingston L, Graham C, Crucian GP, et al. The MoCA: Well‐suited screen for cognitive impairment in Parkinson disease. Neurology 2010;75(19):1717–1725. [DOI] [PubMed] [Google Scholar]
- 15. Quinn JM, Wagner RK. Gender differences in Reading impairment and in the identification of impaired readers: Results from a large‐scale study of At‐risk readers. J Learn Disabil 2015;48(4):433–445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Rianto A. Examining gender differences in reading strategies, reading skills, and English proficiency of EFL university students. Cogent Educ 2021;8(1):1993531. [Google Scholar]
- 17. Aarsland D, Bronnick K, Williams‐Gray C, et al. Mild cognitive impairment in Parkinson disease: A multicenter pooled analysis. Neurology 2010;75(12):1062–1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Grossman M. Sentence processing in Parkinson's disease. Brain Cogn 1999;40(2):387–413. [DOI] [PubMed] [Google Scholar]
- 19. Fernández G, Laubrock J, Mandolesi P, Colombo O, Agamennoni O. Registering eye movements during reading in Alzheimer's disease: Difficulties in predicting upcoming words. J Clin Exp Neuropsychol 2014;36(3):302–316. [DOI] [PubMed] [Google Scholar]
- 20. Choi W, Desai RH, Henderson JM. The neural substrates of natural reading: A comparison of normal and nonword text using eyetracking and fMRI. Front Hum Neurosci 2014;8:1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Rieger JW, Kim A, Argyelan M, et al. Cortical functional anatomy of voluntary saccades in Parkinson disease. Clin EEG Neurosci 2008;39(4):169–174. [DOI] [PubMed] [Google Scholar]
- 22. Chaudhary S, Kumaran SS, Goyal V, et al. Frontal lobe metabolic alterations characterizing Parkinson's disease cognitive impairment. Neurol Sci 2021;42(3):1053–1064. [DOI] [PubMed] [Google Scholar]
- 23. Srivastava A, Sharma R, Goyal V, Chaudhary S, Sood SK, Kumaran SS. Saccadic eye movements in young‐onset Parkinson's disease ‐ a BOLD fMRI study. Neuroophthalmology 2020;44(2):89–99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Jehangir N, Yu CY, Song J, et al. Slower saccadic reading in Parkinson's disease. PLoS One 2018;13(1):e0191005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Mathis T, Rauber H, Sautivet L, Chambard C, Denis P, Danaila T, Kodjikian L. Screening for reading difficulties in Parkinson's disease: An evaluation of the Alouette test. J Fr Ophtalmol 2018;41(8):718–724. [DOI] [PubMed] [Google Scholar]
