Oculomotor behavior of blind patients seeing with a subretinal visual implant

Electronic implants are able to restore some visual function in blind patients with hereditary retinal degenerations. Subretinal visual implants, such as the CE-approved Retina Implant Alpha IMS (Retina Implant AG, Reutlingen, Germany), sense light through the eye's optics and subsequently stimulate retinal bipolar cells via ∼1500 independent pixels to project visual signals to the brain. Because these devices are directly implanted beneath the fovea, they potentially harness the full benefit of eye movements to scan scenes and fixate objects. However, so far, the oculomotor behavior of patients using subretinal implants has not been characterized. Here, we tracked eye movements in two blind patients seeing with a subretinal implant, and we compared them to those of three healthy controls. We presented bright geometric shapes on a dark background, and we asked the patients to report seeing them or not. We found that once the patients visually localized the shapes, they fixated well and exhibited classic oculomotor fixational patterns, including the generation of microsaccades and ocular drifts. Further, we found that a reduced frequency of saccades and microsaccades was correlated with loss of visibility. Last, but not least, gaze location corresponded to the location of the stimulus, and shape and size aspects of the viewed stimulus were reflected by the direction and size of saccades. Our results pave the way for future use of eye tracking in subretinal implant patients, not only to understand their oculomotor behavior, but also to design oculomotor training strategies that can help improve their quality of life.

[1]  M. Ashburner,et al.  Shape Representations and Visual Guidance of Saccadic Eye Movements , 2022 .

[2]  Ziad M. Hafed,et al.  On the Dissociation between Microsaccade Rate and Direction after Peripheral Cues: Microsaccadic Inhibition Revisited , 2013, The Journal of Neuroscience.

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

[4]  Ziad M. Hafed,et al.  Active Vision: Microsaccades Direct the Eye to Where It Matters Most , 2013, Current Biology.

[5]  Martina Poletti,et al.  Stability of the Visual World during Eye Drift , 2010, The Journal of Neuroscience.

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

[7]  F A Miles,et al.  Release of fixation for pursuit and saccades in humans: evidence for shared inputs acting on different neural substrates. , 1996, Journal of neurophysiology.

[8]  Eberhart Zrenner,et al.  Fighting Blindness with Microelectronics , 2013, Science Translational Medicine.

[9]  Eberhart Zrenner,et al.  Functional outcome in subretinal electronic implants depends on foveal eccentricity. , 2013, Investigative ophthalmology & visual science.

[10]  Robert Sekuler,et al.  Geometric structure and chunking in reproduction of motion sequences. , 2008, Journal of vision.

[11]  Nikos K. Logothetis,et al.  Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex , 1998, Experimental Brain Research.

[12]  Ralf Engbert,et al.  Microsaccades uncover the orientation of covert attention , 2003, Vision Research.

[13]  R. Reid,et al.  Saccadic Eye Movements Modulate Visual Responses in the Lateral Geniculate Nucleus , 2002, Neuron.

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

[15]  Jessy D. Dorn,et al.  Interim results from the international trial of Second Sight's visual prosthesis. , 2012, Ophthalmology.

[16]  L. Riggs,et al.  The disappearance of steadily fixated visual test objects. , 1953, Journal of the Optical Society of America.

[17]  Vision Research , 1961, Nature.

[18]  Alfred Stett,et al.  Subretinal electronic chips allow blind patients to read letters and combine them to words , 2010, Proceedings of the Royal Society B: Biological Sciences.

[19]  Alexander Pastukhov,et al.  Spatial and temporal attention revealed by microsaccades , 2013, Vision Research.

[20]  James J. Clark,et al.  Microsaccades as an overt measure of covert attention shifts , 2002, Vision Research.

[21]  Chih-Yang Chen,et al.  Postmicrosaccadic Enhancement of Slow Eye Movements , 2013, The Journal of Neuroscience.

[22]  E. Zrenner Will Retinal Implants Restore Vision ? , 2002 .

[23]  P. Boyce,et al.  The effect of flicker on eye movements , 1968 .

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

[25]  T Moore,et al.  Shape representations and visual guidance of saccadic eye movements. , 1999, Science.

[26]  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.

[27]  F. Amthor,et al.  Retinal ganglion cell coding in simulated active vision , 2005, Visual Neuroscience.

[28]  G. Karmos,et al.  Transient cortical excitation at the onset of visual fixation. , 2008, Cerebral cortex.

[29]  J. Braun,et al.  Rare but precious: Microsaccades are highly informative about attentional allocation , 2010, Vision Research.

[30]  B. L. Zuber,et al.  Microsaccades and the Velocity-Amplitude Relationship for Saccadic Eye Movements , 1965, Science.

[31]  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.

[32]  Michael J. Berry,et al.  Role of eye movements in the retinal code for a size discrimination task. , 2007, Journal of neurophysiology.

[33]  Dave M. Stampe,et al.  Heuristic filtering and reliable calibration methods for video-based pupil-tracking systems , 1993 .

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

[35]  S. Feldon,et al.  Square‐wave jerks , 1977, Neurology.

[36]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[37]  Angelika Braun,et al.  Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS , 2013, Proceedings of the Royal Society B: Biological Sciences.

[38]  Richard V Abadi,et al.  The characteristics of dynamic overshoots in square-wave jerks, and in congenital and manifest latent nystagmus , 2000, Vision Research.

[39]  P R Boyce,et al.  The effect of flicker on eye movement. , 1968, Vision research.

[40]  Roland Thewes,et al.  Electrical stimulation of retinal neurons in epiretinal and subretinal configuration using a multicapacitor array. , 2012, Journal of neurophysiology.

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

[42]  Farhad Hafezi,et al.  Temporal properties of visual perception on electrical stimulation of the retina. , 2012, Investigative ophthalmology & visual science.

[43]  F. J. Verheijen,et al.  Mechanism of Visual Autokinesis , 1964, Nature.

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

[45]  Ziad M. Hafed,et al.  Microsaccadic Suppression of Visual Bursts in the Primate Superior Colliculus , 2010, Journal of Neuroscience.