A compact field guide to the study of microsaccades: Challenges and functions

Following a period of quiescence at the end of last century, the study of microsaccades has now regained strong impetus and broad attention within the vision research community. This wave of interest, partly fueled by the advent of user-friendly high-resolution eyetrackers, has attracted researchers and led to novel ideas. Old hypothesis have been revisited and new ones formulated. This article is designed to serve as a practical guide for researchers in the field. Because of the history of the field and the difficulty of measuring very small eye movements, the study of microsaccades presents peculiar challenges. Here, we summarize some of the main challenges and describe methods for assessing and improving the quality of the recordings. Furthermore, we examine how these experimental challenges have influenced analysis of the visual functions of microsaccades and critically review current evidence on three long-debated proposals: the maintenance of fixation, the prevention of visual fading, and the exploration of fine spatial detail.

[1]  J. Victor,et al.  Temporal Encoding of Spatial Information during Active Visual Fixation , 2012, Current Biology.

[2]  M. A. Goodale,et al.  What is the best fixation target? The effect of target shape on stability of fixational eye movements , 2013, Vision Research.

[3]  Barbara J. Winterson,et al.  Microsaccades during finely guided visuomotor tasks , 1976, Vision Research.

[4]  Xoana G. Troncoso,et al.  Microsaccadic efficacy and contribution to foveal and peripheral vision , 2012 .

[5]  P. Blignaut,et al.  Eye-tracking data quality as affected by ethnicity and experimental design , 2014, Behavior research methods.

[6]  Mark M J Houben,et al.  Recording three-dimensional eye movements: scleral search coils versus video oculography. , 2006, Investigative ophthalmology & visual science.

[7]  J NACHMIAS,et al.  Two-dimensional motion of the retinal image during monocular fixation. , 1959, Journal of the Optical Society of America.

[8]  Frank Schaeffel,et al.  Variations of pupil centration and their effects on video eye tracking , 2013, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[9]  Zygmunt Pizlo,et al.  One fixates accurately in order to see clearly not because one sees clearly. , 2003, Spatial vision.

[10]  Alan Kennedy,et al.  Book Review: Eye Tracking: A Comprehensive Guide to Methods and Measures , 2016, Quarterly journal of experimental psychology.

[11]  H D Crane,et al.  Generation-V dual-Purkinje-image eyetracker. , 1985, Applied optics.

[12]  M. Rucci,et al.  Microsaccades Precisely Relocate Gaze in a High Visual Acuity Task , 2010, Nature Neuroscience.

[13]  D Purves,et al.  The extraordinarily rapid disappearance of entoptic images. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Vision Research , 1961, Nature.

[15]  G. W. Beeler,et al.  Visual threshold changes resulting from spontaneous saccadic eye movements. , 1967, Vision research.

[16]  Xoana G. Troncoso,et al.  Microsaccades Counteract Visual Fading during Fixation , 2005, Neuron.

[17]  Heiner Deubel,et al.  Perceptual consequences of ocular lens overshoot during saccadic eye movements , 1995, Vision Research.

[18]  Martina Poletti,et al.  Eye movements under various conditions of image fading. , 2010, Journal of vision.

[19]  Ziad M. Hafed,et al.  Similarity of superior colliculus involvement in microsaccade and saccade generation. , 2012, Journal of neurophysiology.

[20]  A. Hendrickson,et al.  Human photoreceptor topography , 1990, The Journal of comparative neurology.

[21]  Ziad M. Hafed Alteration of Visual Perception prior to Microsaccades , 2013, Neuron.

[22]  Eileen Kowler,et al.  The eye on the needle , 2010, Nature Neuroscience.

[23]  Maynard C. Wheeler,et al.  VISUAL ACUITY WITHIN THE AREA CENTRALIS AND ITS RELATION TO EYE MOVEMENTS AND FIXATION , 1928 .

[24]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[25]  Austin Roorda,et al.  Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy , 2005 .

[26]  Ziad M. Hafed,et al.  A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus , 2009, Science.

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

[28]  B. Bridgeman,et al.  The role of microsaccades in high acuity observational tasks , 1980, Vision Research.

[29]  R. Steinman,et al.  Small saccades serve no useful purpose: Reply to a letter by R. W. Ditchburn , 1980, Vision Research.

[30]  Pierre Baldi,et al.  The role of bottom-up and top-down influences in directing primate gaze shifts , 2010 .

[31]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[32]  R. W. DITCHBURN,et al.  Vision with a Stabilized Retinal Image , 1952, Nature.

[33]  Michael H Herzog,et al.  Different types of feedback change decision criterion and sensitivity differently in perceptual learning. , 2012, Journal of vision.

[34]  A. A. Skavenski,et al.  Quality of retinal image stabilization during small natural and artificial body rotations in man , 1979, Vision Research.

[35]  Michele Rucci,et al.  EyeRIS: A general-purpose system for eye-movement-contingent display control , 2007, Behavior research methods.

[36]  P. Wurtz,et al.  Size Matters: Saccades during Scene Perception , 2007, Perception.

[37]  D. Snodderly,et al.  Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion, position, and extraretinal influences. , 2008, Journal of vision.

[38]  H J Gerrits,et al.  Artificial movements of a stabilized image. , 1970, Vision research.

[39]  R. Steinman,et al.  Voluntary Control of Microsaccades during Maintained Monocular Fixation , 1967, Science.

[40]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[41]  Reinhold Kliegl,et al.  Microsaccadic modulation of response times in spatial attention tasks , 2009, Psychological research.

[42]  M. Rucci,et al.  Contributions of fixational eye movements to the discrimination of briefly presented stimuli. , 2003, Journal of vision.

[43]  H. Collewijn,et al.  Precise recording of human eye movements , 1975, Vision Research.

[44]  Joan Parkinson,et al.  Eye Movement Abnormalities in Alzheimer Disease: Case Presentation and Literature Review , 2005, The American orthoptic journal.

[45]  H. Collewijn,et al.  The significance of microsaccades for vision and oculomotor control. , 2008, Journal of vision.

[46]  M. Rolfs Microsaccades: Small steps on a long way , 2009, Vision Research.

[47]  Randolph Blake,et al.  Correcting video-based eye tracking signals for pupil size artifacts , 2014 .

[48]  P. Boyce Monocular fixation in human eye movement , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[49]  P C Garell,et al.  A case report on fixation instability in Parkinson’s disease with bilateral deep brain stimulation implants , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[50]  R. W. Ditchburn,et al.  What is psychophysically perfect image stabilization? Do perfectly stabilized images always disappear?: comment. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[51]  D. Fender,et al.  The interplay of drifts and flicks in binocular fixation. , 1969, Vision research.

[52]  R. W. Ditchburn,et al.  Involuntary eye movements during fixation , 1953, The Journal of physiology.

[53]  Paul R. Martin,et al.  Receptive field asymmetries produce color-dependent direction selectivity in primate lateral geniculate nucleus. , 2010, Journal of vision.

[54]  R. Steinman,et al.  The smallest voluntary saccade: implications for fixation. , 1973, Vision research.

[55]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[56]  T. Cornsweet Determination of the stimuli for involuntary drifts and saccadic eye movements. , 1956, Journal of the Optical Society of America.

[57]  Z Pizlo,et al.  When push comes to shove: compensation for passive perturbation of the head during natural gaze shifts. , 1995, Journal of vestibular research : equilibrium & orientation.

[58]  Harry J. Wyatt,et al.  The human pupil and the use of video-based eyetrackers , 2010, Vision Research.

[59]  U. Tulunay-Keesey,et al.  Fading of stabilized retinal images. , 1982, Journal of the Optical Society of America.

[60]  Naghmeh Mostofi,et al.  Are the visual transients from microsaccades helpful? Measuring the influences of small saccades on contrast sensitivity , 2016, Vision Research.

[61]  K J Ciuffreda,et al.  Fixational eye movements in amblyopia and strabismus. , 1979, Journal of the American Optometric Association.

[62]  M. Rucci,et al.  Precision of sustained fixation in trained and untrained observers. , 2012, Journal of vision.

[63]  Marcus Nyström,et al.  The influence of calibration method and eye physiology on eyetracking data quality , 2013, Behavior research methods.

[64]  Michele Rucci,et al.  The Visual Input to the Retina during Natural Head-Free Fixation , 2014, The Journal of Neuroscience.

[65]  J J Koenderink,et al.  Contrast enhancement and the negative afterimage. , 1972, Journal of the Optical Society of America.

[66]  K. Cullen,et al.  Coding of Microsaccades in Three-Dimensional Space by Premotor Saccadic Neurons , 2012, The Journal of Neuroscience.

[67]  Martina Poletti,et al.  Microscopic Eye Movements Compensate for Nonhomogeneous Vision within the Fovea , 2013, Current Biology.

[68]  R. W. Ditchburn,et al.  Vision with controlled movements of the retinal image , 1959, The Journal of physiology.

[69]  R. Steinman,et al.  Comparison of saccadic eye movements during fixation and reading. , 1969, Vision research.

[70]  Vincent Hayward,et al.  Discrete-time adaptive windowing for velocity estimation , 2000, IEEE Trans. Control. Syst. Technol..

[71]  D Wyman,et al.  The oculomotor error signal in the fovea. , 1972, Vision research.

[72]  D H Kelly,et al.  Motion and vision. I. Stabilized images of stationary gratings. , 1979, Journal of the Optical Society of America.

[73]  Claudio M. Privitera,et al.  Analysis of microsaccades and pupil dilation reveals a common decisional origin during visual search , 2014, Vision Research.

[74]  B. Winn,et al.  The effect of abnormal fixational eye movements upon visual acuity in congenital nystagmus. , 1999, Current eye research.

[75]  Jeff B. Pelz,et al.  Compensating for eye tracker camera movement , 2006, ETRA.

[76]  R. C. Emerson,et al.  Paralysis of the awake human: Visual perceptions , 1976, Vision Research.

[77]  Ralf Engbert,et al.  Microsaccades Keep the Eyes' Balance During Fixation , 2004, Psychological science.

[78]  D. Munoz,et al.  A neural correlate for the gap effect on saccadic reaction times in monkey. , 1995, Journal of neurophysiology.

[79]  R. Steinman,et al.  Characteristics of saccades and vergence in two kinds of sequential looking tasks , 2000, Vision Research.

[80]  Todd M. Herrington,et al.  The Effect of Microsaccades on the Correlation between Neural Activity and Behavior in Middle Temporal, Ventral Intraparietal, and Lateral Intraparietal Areas , 2009, The Journal of Neuroscience.

[81]  A. Sjølie,et al.  The contribution of microsaccades and drifts in the maintenance of binocular steady fixation , 2006, Graefe's Archive for Clinical and Experimental Ophthalmology.

[82]  A. A. Skavenski,et al.  Miniature eye movement. , 1973, Science.

[83]  Martina Poletti,et al.  Miniature eye movements enhance fine spatial detail , 2007, Nature.

[84]  Ziad M. Hafed,et al.  Visual Fixation as Equilibrium: Evidence from Superior Colliculus Inactivation , 2012, The Journal of Neuroscience.

[85]  A. Vighetto,et al.  Persistent ocular motor manifestations and related visual consequences in multiple sclerosis , 2011, Annals of the New York Academy of Sciences.

[86]  Richard V Abadi,et al.  Visual resolution limits in human albinism , 1991, Vision Research.

[87]  David Williams,et al.  The locus of fixation and the foveal cone mosaic. , 2005, Journal of vision.

[88]  L E Arend,et al.  What is psychophysically perfect image stabilization? Do perfectly stabilized images always disappear? , 1986, Journal of the Optical Society of America. A, Optics and image science.

[89]  Kenneth J. Pope,et al.  Visual Experiences during Paralysis , 2011, Front. Hum. Neurosci..

[90]  D Wyman,et al.  Letter: Latency characteristics of small saccades. , 1973, Vision research.

[91]  M. Turatto,et al.  Visual oddballs induce prolonged microsaccadic inhibition , 2007, Experimental Brain Research.

[92]  K. Shapiro,et al.  The contingent negative variation (CNV) event-related potential (ERP) predicts the attentional blink , 2008 .

[93]  J. Nachmias Determiners of the drift of the eye during monocular fixation. , 1961, Journal of the Optical Society of America.

[94]  Katharina Havermann,et al.  Fine-Scale Plasticity of Microscopic Saccades , 2014, The Journal of Neuroscience.

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

[96]  M Millodot,et al.  Variation of visual acuity in the central region of the retina. , 1972, The British journal of physiological optics.

[97]  R. W. Ditchburn,et al.  Assembled data in eye movements. , 1967, Optica acta.