Eye Movement Abnormalities in Glaucoma Patients: A Review

Figures & data

Figure 1 Schematic representation of trans-synaptic degeneration. Retinal ganglion cell atrophy leads to anterograde trans-synaptic degeneration along the optic nerve, optic tract, LGN, and optic radiation. Emerging theories suggest degeneration beyond these pathways, but this remains controversial.

Figure 2 Schematic representation of trans-synaptic degeneration on a cellular scale.

Figure 3 Efferent control of eye movement. (A) anterior (B) axial and (C) sagittal views of the anatomical origins of cranial nerves III, IV, and VI.

Figure 4 Depiction of a prosacadde, anti-saccade, and fixation task.

Figure 5 Forest plot of saccade latency as measured in milliseconds.^62–67,171

Figure 6 Forest plot of peak saccade velocity data as measured by degrees/ second. Ballae et al⁶³ report their velocities as degrees/ millisecond which is interpreted by the authors as a misprint.^62,63,66

Figure 7 Forest plot of fixation task data as measured by log-BCEA 95%. *Longhin et al⁹⁸ did not report their range of BCEA values which provides a misleading effect size in this figure.^86,98,99

Table 1 Studies on Isolated Saccade and Anti-Saccade Tasks in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Ballae et al 2020.^Citation63	37 glaucoma patients aged 61 ± 10 (15 POAG, 14 PACG, 8 NTG) 15 controls age 55 ±8 (not age-matched)	Static peripheral saccade target* at 5, 7, and 10 degrees from fixation	Longer latency, reduced velocity and hypometric saccades in glaucoma groups (particularly NTG)
Kanjee et al 2012.^Citation62	16 POAG aged 60.9 ± 8.13 21 controls aged 63.2 ± 8.7 (age-matched)	Static peripheral saccade target* at 0 and 10 degrees from fixation	Longer latency and decreased express saccades in glaucoma. No difference between groups for saccade duration, amplitude or velocity
Lamirel et al 2014.^Citation64	8 POAG (consisting of 4 preperimetric glaucoma patients aged 48–66 and 4 perimetric ‘moderate’ glaucoma aged 37–62) 4 controls aged 44–66,	Static peripheral saccade target* Moving peripheral stimulus (protocol similar to above with moving instead of stationary target)	Static: increased latency and decreased gain in glaucoma Moving: longer latency and poorer accuracy in glaucoma (worse in moderate POAG)
Mazumdar et al 2014.^Citation65	25 perimetric glaucoma (early, moderate, and severe) grouped via age deciles for comparison 30–39, 40–49, and >50 54 controls (age-matched)	Static peripheral saccade target* in varied eccentricities	Prolonged reaction time at all eccentricities in glaucoma groups, worse with increasing disease severity
Mazumdar et al 2021.^Citation171	15 mild glaucoma patients, and 15 moderate (mean age 53; SD 13) in evaluation phase (phase two) of the study 30 controls (mean age 45; SD 13),	Static peripheral saccade target* within standard automated perimetry	Increased reaction time in glaucoma (varied depending on hemifield location)
Najjar et al 2017.^Citation66	16 preperimetric POAG 16 controls (age-matched, 65.5 ± 14.3)	Static peripheral saccade target* at 5, 10, 15, and 20 degrees from fixation Anti-saccade task	Increased latencies, reduced gain, reduced amplitude at all targets, higher anti-saccade errors in glaucoma group.
Tatham et al 2020.^Citation67	31 perimetric glaucoma aged 72.3 ± 7.9 ** 23 controls (not age-matched; aged 65.9 ± 5.6)	Static peripheral saccade target*	Reduced velocities, increased latencies, decreased accuracy in glaucoma, correlated to disease severity
Thepass et al 2021.^Citation75	76 POAG and PACG glaucoma eyes: mild n=32 (mean age 66.5, MD −2.5), moderate n= 15 (mean age 67.9, MD −9.6), advanced n=29 (mean age 68.3, MD −17.6) 58 control eyes (mean age 65.5)	Eye movement perimetry (54-point) with 24–2 visual field	Saccade latency increased (even in areas of preserved visual field) with glaucoma severity which was also correlated to stimulus intensity and eccentricity.

Notes: *static Peripheral Stimulus: Participants View a Central Fixation Point, Which is Extinguished After a Randomised Time Period (Within a Range of a Few Seconds) and a Stationary Saccade Target Appears in the Periphery. Participants are Asked to Look Immediately to the Saccade Target and Then Back to the Central Fixation Stimulus When It Appears. **Where type of glaucoma is not specified, this was not reported in the original paper.

Table 2 Studies on Isolated Fixation Tasks in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Kameda et al 2009.^Citation105	39 advanced glaucoma patients with fixation-threatening scotomas (mean age 66.7 ± 8.8). No control group.	Microperimetry fixation task (using MP-1, Nidek, Japan)	Stable fixation in 37 eyes infixation test (32 with foveal, others paracentral). With MP, 30 eyes showed stable fixation (26 foveal, 13 paracentral). Superior and superotemporal to fovea was preferred when eccentric fixation occurred
Longhin et al 2013.^Citation98	35 eyes with POAG of mean age 59.3 ± 13.6 (range, 37–85). 109 control eyes of mean age 62.8 ± 14.6 (range, 30–86).	Microperimetry fixation task (using MP-1, Nidek, Japan)	POAG group: 88.6% maintained fixation stability in static fixation and 11.4% achieved this in dynamic fixation during MP (significant). BCEA analysis did not reveal a difference between groups.
Montesano et al 2018.^Citation99	103 glaucoma (age 71.14 ± 9.07)** 189 controls not age-matched (age 49.9 ± 15.21)	Compass perimeter fixation task	Sequential Euclidean Distance significantly increased in glaucoma patients during fixation. BCEA-95% and Mean Euclidean Distance was equivocal
Shi et al 2013.^Citation100	23 POAG (age 58.7± 17.8) 13 controls (age 54.0± 14.7)	Microperimetry (MP-1) fixation task	Decreased macular sensitivity and fixation stability in early-moderate POAG. MP-1ʹs classification of fixation stability was not found to be scientifically robust
Zabel et al 2022.^Citation86	32 eyes with mild POAG (age 69.1 ± 8.7) 22 eyes with moderate/severe POAG (age 71.1 ± 8.5) 23 control eyes (age 67.9 ± 7.6)	Microperimetry fixation task (using MAIA MP, Centervue, Italy)	Decreased fixation stability occurred with disease progression. Secondary structural analysis showed deterioration in superficial vascular complex, retinal ganglion cell layer, and peripapillary capillaries with increasing disease severity.

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Table 3 Studies on Optokinetic Nystagmus in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Tong et al 2002.^Citation122	11 perimetric POAG eyes (aged 50–76) 14 control eyes (aged 51–74, and 1 <age 40)	Elicitation of forward, dual-directional, and reverse OKN with different interstimulus interval (ISI) duration and luminance contrast	Varying ISI duration: Almost all POAG eyes showed forward OKN and scarce reverse OKN (contrary to controls). As ISI increased, POAG eyes’ forward OKN deteriorated quicker than control Different luminance contrast: Forward OKN required contrast >10%. Reverse OKN was scarcely evoked at any contrast level in POAG eyes, contrary to control
Shin et al 2006.^Citation121	27 glaucoma eyes** aged 55.7± 13, with 146 eyes of separate, varied pathology	Horizontal optokinetic stimuli for induction and suppression stimuli (vertical stripes)	Induction OKN: Minimum stripe stimulus for OKN was correlated with subjective VA for all patients. All eyes with a visual acuity better than 20/60 (>logMAR0.5) showed OKN response to thinnest stripe width Suppression OKN: 19 glaucoma eyes showed OKN response which correlated to minimum dot size. No patients worse than logMAR 1 (20/200) elicited OKN to suppression stimuli
Abe et al 1993.^Citation123	104 eyes of ocular hypertension and POAG (age 16–74 years, Aulhorn’s stages I–IV of perimetric glaucoma) 110 age-matched controls	Horizontal optokinetic stimuli for induction stimuli (vertical stripes)	Subjective contrast sensitivity was improved with horizontal OKN. Higher sensitivity for minor optic nerve damage was observed with drifting stimulus rather than stationary
Severt et al 2000.^Citation119	8 POAG suspects (ages not specified) 10 controls “roughly age-matched”	Slow phase OKN using spatial frequency doubling illusion	Select variables included in a model achieved 90% accuracy in diagnosing early POAG compared to controls: mean rate of OKN beats, and mean rate of OKN beats occurring within contiguous clusters. Near-FD stimuli produced least age-dependent (and most accurate) results

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Abbreviation: FD, frequency-doubling.

Table 4 Studies on Eye Movements During Reading in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Burton et al 2014.^Citation132	18 advanced glaucoma** (age 71 ± 7) with bilateral VF defects 39 controls (age 67 ± 8)	Reading task: paragraphs of text. Lexical decision task (LDT): real vs false word	Perceptual span^† positively correlated to reading speed in both groups. Saccadic frequency positively correlated to LDT in glaucoma, but not controls. Glaucoma showed higher text saturation^††
Murata et al 2017.^Citation101	50 perimetric glaucoma** (age 52.2 ± 11.4) 20 controls (age 46.9 ± 17.2)	Freely read paragraphs of text in Japanese (horizontal direction)	Glaucoma had longer fixation duration, positively correlated to mean deviation in patient’s worse eye
Smith et al 2014.^Citation135	14 asymmetric POAG (within-person study), mean age 69 (range 64–81)	Freely read paragraphs of text comparing worst eye to better eye	Reading duration and saccade rate were higher in the worse eye. Differences were independent of size and difference in VF loss between both eyes, but rather contrast sensitivity and VA
Burton et al 2012.^Citation131	53 perimetric glaucoma, POAG and NTG (age 66 ± 9) 40 controls (69 ± 8)	Freely read paragraphs of text (16 short paragraphs, eight at 100% contrast and eight at 20% contrast) for speed	Glaucoma patients showed reduced reading speed at lower contrast which correlated to disease severity (VA and VF). No difference in reading speeds between the two groups at 100% contrast
Ishi 2013.^Citation134	49 early-moderate perimetric glaucoma (age 53.3 ± 12.6). 22 POAG, 22 NTG, 4 developmental glaucoma, 1 exfoliation glaucoma 30 controls (age-matched)	Freely read 30 sentences in MNREAD-J (Japanese vertical direction reading) for speed	Glaucoma patients showed reduced reading speed which was positively correlated with VF severity
Cerulli 2013.^Citation133	32 early-moderate POAG. 34 controls (age- and sex-matched)	Freely read two seperate pieces of text (Italian) for both speed (first one) and comprehension (second one)	No difference in reading speed or comprehension between POAG and controls. Maximum eye movement along the horizontal and vertical axes were significantly increased across all stages of glaucoma progression
Ramulu 2009.^Citation2	132 glaucoma (68 unilateral, 64 bilateral) 1017 controls	Freely read aloud short passages of text straight ahead (correctly read words over 15 seconds)	Spoken reading speed was only affected by those with bilateral advanced glaucoma. VA was independent of VF loss
Chen 2021.^Citation144	8 glaucoma (bilateral, mixed-severity) 8 controls	Monocular reading of Malay language standardized test with diminishing print size. Saccade count, fixation count, regressions, and speed were recorded.	Reading speed was reduced in glaucoma patients with an increase in fixation count only. Reading speed was paradoxically decreased with a higher VF defect burden.

Notes: **Where glaucoma subtype is not specified, this was not reported in the original paper. ^†Perceptual span is defined as letters read per number of saccades. ^††Text saturation is defined as the distance between first and last fixation in line of text).

Figure 8 Summary of key points.

Table 5 Studies on Eye Movements During Viewing of, and Searching for Targets Within, Static Images in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Nistal 2020.^Citation138	33 glaucoma** (mean defect 6dB ±5), 23 healthy. Ages not specified	Part a – observation of static images Part b – driving (see Driving)	Glaucoma revealed prolonged visual search, decreased fixations), decreased saccade velocity, and decreased fixations per saccade
Glen et al 2013.^Citation150	51 POAG (n=28 with 10–2 defects aged 70±7, n=23 with 24–2 defects aged 68 ± 8). VA better than 6/9 in all subjects 39 controls aged 66 ± 9	Cambridge Face Memory Test with 1000 Hz eye tracking	Patients with VF defects on 10–2 performed worse on facial recognition than non-10-2 defects and controls. Larger saccades in 10–2 defect group compared with other groups. Significant individual variability noted due to adaptation
Lee et al 2019.^Citation84	31 glaucoma** (aged 71.7 ± 6.3, MD −12 dB in worse eye, −3dB better eye). 25 controls (age-matched)	Report road users present in static images of driving scenes in DriveSafe Test	Shorter fixations on road users and smaller saccades in glaucoma group. Longer road user fixation led to higher DriveSafe test scores
Wiecek et al 2012.^Citation95	10 perimetric glaucoma** aged 68.3 ± 13.6 13 controls aged 64.8 ± 11.3	Monocular viewing for locating a target image in static scene	Glaucoma group showed fewer eye movements toward target area. Saccade directional bias and search performance was not related to VF loss. No difference between groups for total search duration, fixation duration, saccade size, and number of saccade
Smith, Crabb et al, 2012 (a).^Citation94	30 glaucoma, POAG and NTG, with overlapping binocular VF defects aged 68.5 ± 9.7 30 controls aged 68.4 ± 9.5	Freely view static images from natural or urban scenes	Reduced number of saccades, reduced BCEA of fixation, and increased fixation duration in glaucoma. Severity of VF loss and contrast sensitivity impairment was not associated with any eye tracking measures. Saccade amplitude showed large inter-individual variation
Smith, Glen et al, 2012 (b).^Citation149	40 POAG (best eye MD −5.9 ±4 dB) aged 67 ±9 40 controls aged 66 ± 10	Search target within static images of everyday scenes	Reduced saccade rate in glaucoma, correlated to severity of contrast sensitivity impairment and VF loss. Large inter-individual variation in number of saccades.

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Table 6 Studies on Eye Movement During Viewing and Searching for Targets Within Moving Images in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Crabb et al 2010.^Citation83	9 POAG (bilateral) with VA >6/9, aged 67.6 ± 9.3. All experienced drivers 10 controls (aged 64.4 ± 11.4)	Hazard perception test in video clips of driving scenes	More saccades, fixations and missed hazards in POAG, correlated with VF loss.
Crabb et al 2014.^Citation151	44 glaucoma aged 69, IQR 63–77. Early n=9, moderate n=24, advanced n=11 32 controls (mean age 70, IQR 64–75).	Freely viewing TV programmes with scanpaths and saccade density maps analysed via kernel principal component analysis	Eye movement patterns able to diagnose glaucoma with 79% sensitivity and 90% specificity
Lee et al 2017.^Citation93	30 glaucoma** aged 71 ± 7 (better eye MD −3.1 ± 3.2, worse eye MD −11.9 ± 6.2) 25 controls (aged 72 ± 7, 30)	Hazard perception test in video clips of driving scenes, in addition to random-dot kinematograms and drifting Gabor patches for central motion sensitivity	Delayed hazard response times in glaucoma, correlated to motion sensitivity, ‘useful field of view’, and worse eye MD. Glaucoma showed overall smaller saccades. Larger saccades were associated with faster hazard responses in the glaucoma group only.
Asfaw et al 2018.^Citation92	15 asymmetric POAG (MD >6 between both eyes)	Freely view static image from film one eye at a time, in sequence	Saccade amplitude and BCEA decreased and increased saccadic reversal rate in worse eye. Between-eye BCEA values predicted between-eye MD values
Soans et al 2021.^Citation153	15 glaucoma aged 43.9 ± 12.5. POAG n=9, steroid-induced n=2, juvenile n=3, PACG n=1 21 controls aged 38 ± 15.	Smooth pursuit of target on screen with separate task of following target jumping in random sequence	Glaucoma had higher latencies, higher positional errors, and lower velocities relative to controls. During smooth pursuit, there was a higher time lag compared to controls.

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Abbreviation: IQR, interquartile range.

Table 7 Studies on Eye Movements While Walking Through an Environment in Patients with Glaucoma

Paper	Participants	Methods	Summary of Results
Cheong et al 2008.^Citation85	8 patients with visual field defects (3 glaucoma with binocular VF <20 degrees, 5 retinitis pigmentosa) 5 controls (age-matched)	Real-world street crossing task with portable eye tracking. Participants pressed a button when they believed safe to cross the street	Traffic gap identification significantly impaired in patient group with reduction of fixation area
Geruschat et al 2006.^Citation163	12 glaucoma** (age 63.9 ± 12.7 with mean binocular VF of 95 degrees), 9 macular degeneration (aged 78/7 ±6) 12 controls (age 58.6 ± 24.1)	Real-world street crossing task with portable eye tracking. Patients crossed the street and returned	Visually impaired focused on vehicles when crossing rather than traffic lights
Lajoie et al 2018.^Citation161	20 moderate-severe glaucoma (age 74.8 ± 6.5) 20 controls (age 70.5 ± 7)	Navigating an obstacle course (36 trials per participant) with single and dual-task conditions (eg counting backwards whilst walking)	Glaucoma patients walked slower in all conditions with smaller gaze distance and gaze closer to their position and direct fixation to obstacles in front. Multitasking led to increased obstacle contact in glaucoma group
Sippel et al 2014.^Citation162	10 glaucoma (advanced binocular VF loss, aged 60.7 ± 8.7) 10 controls (age 59.9 ± 9.1)	Real-world supermarket task: collect specific products from shelves as quickly as possible	Glaucoma patients showed longer search times with frequent glancing to visual field defect as a compensatory mechanism
Dive et al 2016.^Citation164	13 POAG (bilateral MD worse than/ equal to −6 dB, ages 31–81) 13 controls (age 73.3 ± 9.1)	Sandwich-making task and building task with children’s playset	Glaucoma patients were slower on building task. Increased fixation durations and frequency of saccades in POAG

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Table 8 Studies on Eye Movements During Driving in Patients with Glaucoma

Paper	Participants	Methods	Did Participants Meet Legal Driving Standards?	Summary of Results
Kasneci et al 2014.^Citation136	10 POAG (advanced bilateral field loss, age 60.7 ± 8.7), 10 homonymous field defects from non-glaucomatous causes 20 controls (age 59.9 ± 9.1)	On-road driving test, 20km. German legal standard	All glaucoma subjects held a valid driving license. 6/10 glaucoma failed to pass driving test and 4/10 did not meet legal driving requirements, but passed the test	Severity of VF loss correlated to poor lane changing, driving around curves, and predicting hazards. Proportion of glances to visual field defects was correlated to its size. Those who passed had increased head and shoulder movements
Kübler et al 2015.^Citation96	6 POAG (age 61.5, IQR 52–71) 8 controls (age/sex-matched)	Advanced moving-base driving simulator testing. German legal standard	3/6 glaucoma patients passed the test. None met the legal driving requirements	Those who passed had larger saccades, more vertical scanning, and increased head movements compared to controls
Lee et al 2018.^Citation137	13 glaucoma** (age 72 ± 6.7, better-eye MD 2.9 ± 2.1, worse-eye MD −12.5±7.1) 10 controls (age 70.6 ± 7.4)	Closed-road circuit	Not evaluated	Poorer driving scores, increased collisions, larger saccades in glaucoma group. Better-eye MD was strongest predictor for driving score
Nistal 2020.^Citation138	33 glaucoma** (mean defect 6dB ±5) 23 control. Ages not specified	Part a - observation of static images (see Static Images) Part b - On-screen driving simulator	Not evaluated	Hypometric saccades and decreased velocities with a higher number of collisions in glaucoma group
Prado Vega et al 2013.^Citation97	23 POAG (age 65.1 ±12.2, left MD −13.99 ± 7.04, right MD −10.72±8.98) 12 controls (age 65.7 ± 9.4)	Fixed-base driving simulator Included both driving and letter recognition tasks	Not evaluated	Increased steering activity and missed more letters in glaucoma group. No difference between groups for obstacle avoidance

Note: **Where glaucoma subtype is not specified, this was not reported in the original paper.

Abbreviation: IQR, interquartile range.

Table 9 Keywords Included in Search Strategy

Population	Exposure/ Intervention	Outcome
Glaucoma, including primary open glaucoma, primary angle closure glaucoma, normal tension glaucoma, narrow angle glaucoma, perimetric and pre-perimetric	Eye-tracking, eye tracking, eye moments, video-oculography, ocular motor, oculomotor, pupil tracking, pupil-tracking, saccades, saccades, Fixation, optokinetic nystagmus (OKN), driving, reading, static images, moving images, walking through an environment, negotiating obstacles, visual exploration, street crossing, natural actions, smooth pursuit, face test, driving scenes, static scene, hazard perception, static image, obstacle course, supermarket, task, driving simulator	Gain, velocity, latency, amplitude, hypometric, hypermetric, reaction time, BCEA (bivariate contour ellipse area), fixation stability, OKN beats, OKN signal, reading speed, saccade duration, saccade rate, visual search, gaze, euclidean distance, accuracy.

Figure 9 Study selection for review according to PRISMA criteria described in Moher et al 2009.¹⁸¹

Mazumdar D, Meethal NSK, George R, Pel JJM. Saccadic reaction time in mirror image sectors across horizontal Meridian in eye movement perimetry. Sci Rep. 2021;11(1):2630. doi:10.1038/s41598-021-81762-y

 PubMed Web of Science ®Google Scholar

Ballae Ganeshrao S, Jaleel A, Madicharla S, et al. Comparison of saccadic eye movements among the high tension glaucoma, primary angle closure glaucoma, and normal tension glaucoma. J Glaucoma. 2020;2:548.

 Google Scholar

Kanjee R, Yücel YH, Steinbach MJ, González EG, Gupta N. Delayed saccadic eye movements in glaucoma. Eye Brain. 2012;4:63–68. doi:10.2147/EB.S38467

 PubMedGoogle Scholar

Najjar RP, Sharma S, Drouet M, et al. Disrupted Eye movements in preperimetric primary open-angle glaucoma. Invest Opthalmol Visual Sci. 2017;58(4):2430. doi:10.1167/iovs.16-21002

 PubMed Web of Science ®Google Scholar

Longhin E, Convento E, Pilotto E, et al. Static and dynamic retinal fixation stability in microperimetry. Can J Ophthalmol. 2013;48(5):375–380. doi:10.1016/j.jcjo.2013.05.021

 PubMed Web of Science ®Google Scholar

Zabel K, Zabel P, Suwala K, et al. Alterations in fixation indices in primary open-angle glaucoma by microperimetry. J Clin Med. 2022;11(9):2368. doi:10.3390/jcm11092368

 PubMed Web of Science ®Google Scholar

Montesano G, Crabb DP, Jones PR, Fogagnolo P, Digiuni M, Rossetti LM. Evidence for alterations in fixational eye movements in glaucoma. BMC Ophthalmol. 2018;18(1):191. doi:10.1186/s12886-018-0870-7

 PubMed Web of Science ®Google Scholar

Lamirel C, Milea D, Cochereau I, Duong M-H, Lorenceau J. Impaired Saccadic eye movement in primary open-angle glaucoma. J Glaucoma. 2014;23(1):23–32. doi:10.1097/IJG.0b013e31825c10dc

 PubMed Web of Science ®Google Scholar

Mazumdar D, Pel JM, Panday M, et al. Comparison of saccadic reaction time between normal and glaucoma using an eye movement perimeter. Indian J Ophthalmol. 2014;62(1):55. doi:10.4103/0301-4738.126182

 PubMed Web of Science ®Google Scholar

Tatham AJ, Murray IC, McTrusty AD, et al. Speed and accuracy of saccades in patients with glaucoma evaluated using an eye tracking perimeter. BMC Ophthalmol. 2020;20(1):259. doi:10.1186/s12886-020-01528-4

 PubMed Web of Science ®Google Scholar

Thepass G, Lemig H, Vermeer K, Van der Steen J, Pel J. Slowed saccadic reaction times in seemingly normal parts of glaucomatous visual fields. Front Med. 2021;8:679297. doi:10.3389/fmed.2021.679297

 Web of Science ®Google Scholar

Kameda T, Tanabe T, Hangai M, Ojima T, Aikawa H, Yoshimura N. Fixation behavior in advanced stage glaucoma assessed by the MicroPerimeter MP-1. Jpn J Ophthalmol. 2009;53(6):580–587. doi:10.1007/s10384-009-0735-y

 PubMed Web of Science ®Google Scholar

Shi Y, Liu M, Wang X, Zhang C, Huang P. Fixation behavior in primary open angle glaucoma at early and moderate stage assessed by the microPerimeter MP-1:. J Glaucoma. 2013;22(2):169–173. doi:10.1097/IJG.0b013e3182311dce

 PubMed Web of Science ®Google Scholar

Tong J, Wang J, Sun F. Dual-directional optokinetic nystagmus elicited by the intermittent display of gratings in primary open-angle glaucoma and normal eyes. Curr Eye Res. 2002;25(6):355–362. doi:10.1076/ceyr.25.6.355.14236

 PubMed Web of Science ®Google Scholar

Shin YJ, Park KH, Hwang J-M, Wee WR, Lee JH, Lee IB. Objective measurement of visual acuity by optokinetic response determination in patients with ocular diseases. Am J Ophthalmol. 2006;141(2):327–332. doi:10.1016/j.ajo.2005.09.025

 PubMed Web of Science ®Google Scholar

Abe H, Hasegawa S, Takagi M, Yoshizawa T, Usui T. Contrast sensitivity for the stationary and drifting vertical stripe patterns in patients with optic nerve disorders. Ophthalmologica. 1993;207(2):100–105. doi:10.1159/000310413

 PubMed Web of Science ®Google Scholar

Severt W, Maddess T, Ibbotson M. Employing following eye movements to discriminate normal from glaucoma subjects. Clin Experiment Ophthalmol. 2000;28(3):172–174. doi:10.1046/j.1442-9071.2000.00295.x

 PubMed Web of Science ®Google Scholar

Burton R, Smith ND, Crabb DP. Eye movements and reading in glaucoma: observations on patients with advanced visual field loss. Graefe’s Arch Clin Exp Ophthalmol. 2014;252(10):1621–1630. doi:10.1007/s00417-014-2752-x

 PubMed Web of Science ®Google Scholar

Murata N, Miyamoto D, Togano T, Fukuchi T. Evaluating silent reading performance with an eye tracking system in patients with glaucoma. PLoS One. 2017;12(1):e0170230. doi:10.1371/journal.pone.0170230

 PubMed Web of Science ®Google Scholar

Smith ND, Glen FC, Mönter VM, Crabb DP. Using eye tracking to assess reading performance in patients with glaucoma: a within-person study. J Ophthalmol. 2014;2014:1–10. doi:10.1155/2014/120528

 Web of Science ®Google Scholar

Burton R, Crabb DP, Smith ND, Glen FC, Garway-Heath DF. Glaucoma and Reading: exploring the Effects of Contrast Lowering of Text. Optometry Vision Sci. 2012;89(9):1282–1287. doi:10.1097/OPX.0b013e3182686165

 PubMed Web of Science ®Google Scholar

Ishii M, Seki M, Harigai R, Abe H, Fukuchi T. Reading performance in patients with glaucoma evaluated using the MNREAD charts. Jpn J Ophthalmol. 2013;57(5):471–474. doi:10.1007/s10384-013-0259-3

 PubMed Web of Science ®Google Scholar

Cerulli A, Cesareo M, Ciuffoletti E, et al. Evaluation of eye movements pattern during reading process in patients with glaucoma: a microperimeter study. Invest Opthalmol Visual Sci. 2013;6.

 Google Scholar

Ramulu PY. Glaucoma and reading speed: the Salisbury eye evaluation project. Arch Ophthalmol. 2009;127(1):82. doi:10.1001/archophthalmol.2008.523

 PubMedGoogle Scholar

Chen A-H, Jufri S, Congdon N. The impact of glaucomatous visual field defects on speed and eye movements during reading. Siriraj Med J. 2021;73(1):17–25. doi:10.33192/Smj.2021.03

 Google Scholar

Martínez-Almeida Nistal I, Lampreave Acebes P, Martínez-de-la-casa JM, Sánchez-González P. Validation of virtual reality system based on eye-tracking technologies to support clinical assessment of glaucoma. Eur J Ophthalmol. 2020;1:112067212097604.

 Google Scholar

Glen FC, Smith ND, Crabb DP. Saccadic eye movements and face recognition performance in patients with central glaucomatous visual field defects. Vision Res. 2013;82:42–51. doi:10.1016/j.visres.2013.02.010

 PubMed Web of Science ®Google Scholar

Lee SS-Y, Black AA, Wood JM. Eye movements of drivers with glaucoma on a visual recognition slide test. Optometry Vision Sci. 2019;96(7):484–491. doi:10.1097/OPX.0000000000001395

 PubMed Web of Science ®Google Scholar

Wiecek E, Pasquale LR, Fiser J, Dakin S, Bex PJ. Effects of peripheral visual field loss on eye movements during visual search. Front Psychol. 2012;3. doi:10.3389/fpsyg.2012.00472

 PubMed Web of Science ®Google Scholar

Smith ND, Crabb DP, Glen FC, Burton R, Garway-heath david F. Eye movements in patients with glaucoma when viewing images of everyday scenes. Seeing Perceiving. 2012;25(5):471–492. doi:10.1163/187847612X634454

 PubMedGoogle Scholar

Smith ND, Glen FC, Crabb DP. Eye movements during visual search in patients with glaucoma. BMC Ophthalmol. 2012;12(1):45. doi:10.1186/1471-2415-12-45

 PubMed Web of Science ®Google Scholar

Crabb DP, Smith ND, Rauscher FG, et al. Exploring eye movements in patients with glaucoma when viewing a driving scene. PLoS One. 2010;5(3):e9710. doi:10.1371/journal.pone.0009710

 PubMed Web of Science ®Google Scholar

Crabb DP, Smith ND, Zhu H. What’s on TV? Detecting age-related neurodegenerative eye disease using eye movement scanpaths. Front Aging Neurosci. 2014;6. doi:10.3389/fnagi.2014.00312

 PubMed Web of Science ®Google Scholar

Lee SS-Y, Black AA, Wood JM. Effect of glaucoma on eye movement patterns and laboratory-based hazard detection ability. PLoS One. 2017;12(6):e0178876. doi:10.1371/journal.pone.0178876

 PubMed Web of Science ®Google Scholar

Asfaw DS, Jones PR, Mönter VM, Smith ND, Crabb DP. Does Glaucoma alter eye movements when viewing images of natural scenes? A between-eye study. Invest Opthalmol Visual Sci. 2018;59(8):3189. doi:10.1167/iovs.18-23779

 PubMed Web of Science ®Google Scholar

Soans RS, Grillini A, Saxena R, Renken RJ, Gandhi TK, Cornelissen FW. Eye-movement-based assessment of the perceptual consequences of glaucomatous and neuro-ophthalmological visual field defects. Transl Vis Sci Technol. 2021;10(2):1. doi:10.1167/tvst.10.2.1

 PubMed Web of Science ®Google Scholar

Cheong AMY, Geruschat DR, Congdon N. Traffic gap judgment in people with significant peripheral field loss. Optometry Vision Sci. 2008;85(1):26–36. doi:10.1097/OPX.0b013e31815ed6fd

 PubMed Web of Science ®Google Scholar

Geruschat DR, Hassan SE, Turano KA, Quigley HA, Congdon NG. Gaze behavior of the visually impaired during street crossing. Optometry Vision Sci. 2006;83(8):550–558. doi:10.1097/01.opx.0000232219.23362.a6

 PubMed Web of Science ®Google Scholar

Lajoie K, Miller AB, Strath RA, Neima DR, Marigold DS. Glaucoma-related differences in gaze behavior when negotiating obstacles. Transl Vis Sci Technol. 2018;7(4):10. doi:10.1167/tvst.7.4.10

 PubMed Web of Science ®Google Scholar

Sippel K, Kasneci E, Aehling K, et al. Binocular glaucomatous visual field loss and its impact on visual exploration - a supermarket study. PLoS One. 2014;9(8):e106089. doi:10.1371/journal.pone.0106089

 PubMed Web of Science ®Google Scholar

Dive S, Rouland JF, Lenoble Q, Szaffarczyk S, McKendrick AM, Boucart M. Impact of peripheral field loss on the execution of natural actions: a study with glaucomatous patients and normally sighted people. J Glaucoma. 2016;25(10):e889–e896. doi:10.1097/IJG.0000000000000402

 PubMed Web of Science ®Google Scholar

Kasneci E, Sippel K, Aehling K, et al. Driving with binocular visual field loss? A study on a supervised on-road parcours with simultaneous eye and head tracking. PLoS One. 2014;9(2):e87470. doi:10.1371/journal.pone.0087470

 PubMed Web of Science ®Google Scholar

Kübler TC, Kasneci E, Rosenstiel W, et al. Driving with glaucoma: task performance and gaze movements. Optometry Vision Sci. 2015;92(11):1037–1046. doi:10.1097/OPX.0000000000000702

 PubMed Web of Science ®Google Scholar

Lee SS-Y, Black AA, Wood JM. Scanning behavior and daytime driving performance of older adults with glaucoma. J Glaucoma. 2018;27(6):558–565. doi:10.1097/IJG.0000000000000962

 PubMed Web of Science ®Google Scholar

Prado Vega R, Leeuwen PM, Rendón Vélez E, Lemij HG, Winter JCF. Obstacle avoidance, visual detection performance, and eye-scanning behavior of glaucoma patients in a driving simulator: a preliminary study. PLoS One. 2013;8(10):e77294. doi:10.1371/journal.pone.0077294

 PubMed Web of Science ®Google Scholar

Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097

 PubMed Web of Science ®Google Scholar