The saccade main sequence revised: A fast and repeatable tool for oculomotor analysis

Saccades are rapid ballistic eye movements that humans make to direct the fovea to an object of interest. Their kinematics is well defined, showing regular relationships between amplitude, duration, and velocity: the saccadic ’main sequence’. Deviations of eye movements from the main sequence can be used as markers of specific neurological disorders. Despite its significance, there is no general methodological consensus for reliable and repeatable measurements of the main sequence. In this work, we propose a novel approach for standard indicators of oculomotor performance. The obtained measurements are characterized by high repeatability, allowing for fine assessments of inter- and intra-subject variability, and inter-ocular differences. The designed experimental procedure is natural and non-fatiguing, thus it is well suited for fragile or non-collaborative subjects like neurological patients and infants. The method has been released as a software toolbox for public use. This framework lays the foundation for a normative dataset of healthy oculomotor performance for the assessment of oculomotor dysfunctions.

[1]  Peter Kiefer,et al.  An Inverse-Linear Logistic Model of The Main Sequence , 2017, Journal of eye movement research.

[2]  Manuela Chessa,et al.  The Perspective Geometry of the Eye: Toward Image-Based Eye-Tracking , 2012 .

[3]  J. E. Lieberman,et al.  Frequency limitations of the two-point central difference differentiation algorithm , 1982, Biological Cybernetics.

[4]  Dirk P. Kroese,et al.  Kernel density estimation via diffusion , 2010, 1011.2602.

[5]  Marcus Nyström,et al.  Sampling frequency and eye-tracking measures: how speed affects durations, latencies, and more , 2010 .

[6]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[7]  Agostino Gibaldi,et al.  High-resolution eye tracking using scanning laser ophthalmoscopy , 2019, ETRA.

[8]  P. Rolan,et al.  Utility of saccadic eye movement analysis as an objective biomarker to detect the sedative interaction between opioids and sleep deprivation in opioid-naive and opioid-tolerant populations , 2010, Journal of psychopharmacology.

[9]  M. Juhola,et al.  Effect of sampling frequencies on computation of the maximum velocity of saccadic eye movements , 1985, Biological Cybernetics.

[10]  Pamela Federighi,et al.  Differences in saccade dynamics between spinocerebellar ataxia 2 and late-onset cerebellar ataxias. , 2011, Brain : a journal of neurology.

[11]  Ruth E. Hogg,et al.  Individual differences in human eye movements: An oculomotor signature? , 2017, Vision Research.

[12]  D G Cogan,et al.  Rapid eye movements in myasthenia gravis. II. Electro-oculographic analysis. , 1976, Archives of ophthalmology.

[13]  Agostino Gibaldi,et al.  Binocular Eye Movements Are Adapted to the Natural Environment , 2019, The Journal of Neuroscience.

[14]  B. Troost,et al.  The ocular motor defects in progressive supranuclear palsy , 1977, Annals of neurology.

[15]  C. Kennard,et al.  Using saccades as a research tool in the clinical neurosciences , 2004 .

[16]  S. Martinez-Conde,et al.  Neuroscience and Biobehavioral Reviews , 2022 .

[17]  A. Fuchs,et al.  Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. , 1969, Vision research.

[18]  L. Stark,et al.  Disorders in cerebellar ocular motor control. I. Saccadic overshoot dysmetria. An oculographic, control system and clinico-anatomical analysis. , 1976, Brain : a journal of neurology.

[19]  Emilio Salinas,et al.  Saccade metrics reflect decision-making dynamics during urgent choices , 2018, Nature Communications.

[20]  Paolo Inchingolo,et al.  On the Identification and Analysis of Saccadic Eye Movements-A Quantitative Study of the Processing Procedures , 1985, IEEE Transactions on Biomedical Engineering.

[21]  Niels Galley,et al.  Saccadic eye movement velocity as an indicator of (de)activation: A review and some speculations. , 1989 .

[22]  Yanning H. Han,et al.  Evaluating Small Eye Movements in Patients with Saccadic Palsies , 2003, Annals of the New York Academy of Sciences.

[23]  L. Optican,et al.  What clinical disorders tell us about the neural control of saccadic eye movements , 2006 .

[24]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

[25]  M. Lappe,et al.  Saccadic suppression during voluntary versus reactive saccades. , 2017, Journal of vision.

[26]  Agostino Gibaldi,et al.  Effects of guided random sampling of TCCs on blood flow values in CT perfusion studies of lung tumors. , 2015, Academic radiology.

[27]  Colin Downey,et al.  Development of Pursuit of a Random Walk by Infants aged 4 to 17 Week , 2018, Journal of Vision.

[28]  M. Maurin,et al.  REVIEW ARTICLE doi: 10.1111/j.1472-8206.2008.00633.x The Hill equation: a review of its capabilities in pharmacological modelling , 2008 .

[29]  Lawrence Stark,et al.  Predictive Control of Eye Tracking Movements , 1962 .

[30]  D. Robinson.  The mechanics of human saccadic eye movement , 1964, The Journal of physiology.

[31]  Chris Tofallis,et al.  Erratum: A better measure of relative prediction accuracy for model selection and model estimation , 2015, J. Oper. Res. Soc..

[32]  Agostino Gibaldi,et al.  Evaluation of the Tobii EyeX Eye tracking controller and Matlab toolkit for research , 2016, Behavior Research Methods.

[33]  A. Terry Bahill,et al.  Frequency Limitations and Optimal Step Size for the Two-Point Central Difference Derivative Algorithm with Applications to Human Eye Movement Data , 1983, IEEE Transactions on Biomedical Engineering.

[34]  Andrea Canessa,et al.  The Active Side of Stereopsis: Fixation Strategy and Adaptation to Natural Environments , 2017, Scientific Reports.

[35]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. , 1993, Journal of neurophysiology.

[36]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. , 1993, Journal of neurophysiology.

[37]  Andreas Sprenger,et al.  Comparison of saccadic peak velocities between electro-oculography, video-oculography and scleral search coil , 2010 .

[38]  L. Optican,et al.  Model of the control of saccades by superior colliculus and cerebellum. , 1999, Journal of neurophysiology.

[39]  Manuela Chessa,et al.  Descriptor : A dataset of stereoscopic images and ground-truth disparity mimicking human fi xations in peripersonal space , 2017 .

[40]  Martin S. Banks,et al.  Are corresponding points fixed? , 2001, Vision Research.

[41]  Jan Drewes,et al.  Shifts in reported gaze position due to changes in pupil size: ground truth and compensation , 2012, ETRA '12.

[42]  Andreas Sprenger,et al.  Overestimation of saccadic peak velocity recorded by electro-oculography compared to video-oculography and scleral search coil , 2010, Clinical Neurophysiology.

[43]  Lisa M. Oakes,et al.  Advances in Eye Tracking in Infancy Research. , 2012, Infancy : the official journal of the International Society on Infant Studies.

[44]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[45]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[46]  J. V. Gisbergen,et al.  A parametric analysis of human saccades in different experimental paradigms , 1987, Vision Research.

[47]  Jeroen J. Bax,et al.  Variability of the main sequence. , 1993, Investigative ophthalmology & visual science.

[48]  Uday K. Jagadisan,et al.  Removal of inhibition uncovers latent movement potential during preparation , 2017, bioRxiv.

[49]  B. Uitdehaag,et al.  Saccadic fatigability in the oculomotor system , 2019, Journal of the Neurological Sciences.

[50]  R. Baloh,et al.  Quantitative measurement of saccade amplitude, duration, and velocity , 1975, Neurology.

[51]  L F Dell'Osso,et al.  Saccadic velocity characteristics: intrinsic variability and fatigue. , 1979, Aviation, space, and environmental medicine.

[52]  Frans W Cornelissen,et al.  The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[53]  Xoana G. Troncoso,et al.  Microsaccades: a neurophysiological analysis , 2009, Trends in Neurosciences.

[54]  Stefano Ramat,et al.  Characteristic Eye Movements in Ataxia-Telangiectasia-Like Disorder: An Explanatory Hypothesis , 2017, Front. Neurol..

[55]  Roel Wierts,et al.  Measuring Saccade Peak Velocity Using a Low-Frequency Sampling Rate of 50 Hz , 2008, IEEE Transactions on Biomedical Engineering.

[56]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[57]  Peter Thier,et al.  A new motor synergy that serves the needs of oculomotor and eye lid systems while keeping the downtime of vision minimal , 2016, eLife.

[58]  I. Gilchrist,et al.  Evidence for a systematic component within scan paths in visual search , 2006 .

[59]  Susana Martinez-Conde,et al.  Saccades during Attempted Fixation in Parkinsonian Disorders and Recessive Ataxia: From Microsaccades to Square-Wave Jerks , 2013, PloS one.

[60]  Terry A. Bahill,et al.  Variability and development of a normative data base for saccadic eye movements. , 1981, Investigative ophthalmology & visual science.

[61]  A Straube,et al.  Decrease in saccadic performance after many visually guided saccadic eye movements in monkeys. , 1997, Investigative ophthalmology & visual science.

[62]  Austin Roorda,et al.  High-speed, image-based eye tracking with a scanning laser ophthalmoscope , 2012, Biomedical optics express.

[63]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[64]  A. L. I︠A︡rbus.  Eye Movements and Vision , 1967 .

[65]  H. S. Metz,et al.  Ocular saccades in lateral rectus palsy. , 1970, Archives of ophthalmology.

[66]  Emily A. Cooper,et al.  Stereopsis is adaptive for the natural environment , 2015, Science Advances.

[67]  P. O'Suilleabhain,et al.  Quantitative oculographic characterisation of internuclear ophthalmoparesis in multiple sclerosis: the versional dysconjugacy index Z score , 2002, Journal of neurology, neurosurgery, and psychiatry.

[68]  A. Fuchs.  Saccadic and smooth pursuit eye movements in the monkey , 1967, The Journal of physiology.

[69]  S Lebedev,et al.  Square-root relations between main saccadic parameters. , 1996, Investigative ophthalmology & visual science.

[70]  J A Nij Bijvank,et al.  A standardized protocol for quantification of saccadic eye movements: DEMoNS , 2018, PloS one.

[71]  Dorine Vergilino-Perez,et al.  Are there any left-right asymmetries in saccade parameters? Examination of latency, gain, and peak velocity. , 2012, Investigative ophthalmology & visual science.