Electrically elicited visual evoked potentials in Argus II retinal implant wearers.

PURPOSE We characterized electrically elicited visual evoked potentials (eVEPs) in Argus II retinal implant wearers. METHODS eVEPs were recorded in four subjects, and analyzed by determining amplitude and latency of the first two positive peaks (P1 and P2). Subjects provided subjective feedback by rating the brightness and size of the phosphenes. We established eVEP input-output relationships, eVEP variability between and within subjects, the effect of stimulating different areas of the retina, and the maximal pulse rate to record eVEPs reliably. RESULTS eVEP waveforms had low signal-to-noise ratios, requiring long recording times and substantial signal processing. Waveforms varied between subjects, but showed good reproducibility and consistent parameter dependence within subjects. P2 amplitude overall was the most robust outcome measure and proved an accurate indicator of subjective threshold. Peak latencies showed small within-subject variability, yet their correlation with stimulus level and subjective rating were more variable than that of peak amplitudes. Pulse rates of up to (2)/3 Hz resulted in reliable eVEP recordings. Perceived phosphene brightness declined over time, as reflected in P1 amplitude, but not in P2 amplitude or peak latencies. Stimulating-electrode location significantly affected P1 and P2 amplitude and latency, but not subjective percepts. CONCLUSIONS While recording times and signal processing are more demanding than for standard visually evoked potential (VEP) recordings, the eVEP has proven to be a reliable tool to verify retinal implant functionality. eVEPs correlated with various stimulus parameters and with perceptual ratings. In view of these findings, eVEPs may become an important tool in functional investigations of retinal prostheses. (ClinicalTrials.gov number NCT00407602.) Dutch Abstract.

[1]  James D. Weiland,et al.  Visual Prosthesis , 2008, Proceedings of the IEEE.

[2]  F. Gekeler,et al.  Implantation of stimulation electrodes in the subretinal space to demonstrate cortical responses in Yucatan minipig in the course of visual prosthesis development. , 2005, European journal of ophthalmology.

[3]  Jing Wang,et al.  Using independent component analysis to remove artifacts in visual cortex responses elicited by electrical stimulation of the optic nerve , 2012, Journal of neural engineering.

[4]  James D. Weiland,et al.  Interphase gap decreases electrical stimulation threshold of retinal ganglion cells , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[5]  I. Johnstone,et al.  Wavelet Threshold Estimators for Data with Correlated Noise , 1997 .

[6]  Eyal Margalit,et al.  Inner retinal mechanisms engaged by retinal electrical stimulation. , 2006, Investigative ophthalmology & visual science.

[7]  J. Morley,et al.  Implantation of episcleral electrodes via anterior orbitotomy for stimulation of the retina with induced photoreceptor degeneration: an in vivo feasibility study on a conceptual visual prosthesis , 2008, Acta Neurochirurgica.

[8]  E. Zrenner,et al.  Electrical multisite stimulation of the isolated chicken retina , 2000, Vision Research.

[9]  J. Morley,et al.  Multichannel surface recordings on the visual cortex: implications for a neuroprosthesis , 2008, Journal of neural engineering.

[10]  Chris E. Williams,et al.  Evaluation of stimulus parameters and electrode geometry for an effective suprachoroidal retinal prosthesis , 2010, Journal of neural engineering.

[11]  R Quian Quiroga,et al.  Wavelet Transform in the analysis of the frequency composition of evoked potentials. , 2001, Brain research. Brain research protocols.

[12]  Lyndon J. Brown,et al.  Performance analysis of stationary and discrete wavelet transform for action potential detection from sympathetic nerve recordings in humans , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[13]  Xiao-Xin Li,et al.  Influential factors of thresholds for electrically evoked potentials elicited by intraorbital electrical stimulation of the optic nerve in rabbit eyes , 2007, Vision Research.

[14]  S L Graham,et al.  Electroencephalogram-based scaling of multifocal visual evoked potentials: effect on intersubject amplitude variability. , 2001, Investigative ophthalmology & visual science.

[15]  Pengjia Cao,et al.  Spatiotemporal properties of multipeaked electrically evoked potentials elicited by penetrative optic nerve stimulation in rabbits. , 2011, Investigative ophthalmology & visual science.

[16]  E. Margalit,et al.  Inner and outer retinal mechanisms engaged by epiretinal stimulation in normal and rd mice , 2011, Visual Neuroscience.

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

[18]  Jean Delbeke,et al.  Measurement of evoked potentials after electrical stimulation of the human optic nerve. , 2010, Investigative ophthalmology & visual science.

[19]  S. J. Kim,et al.  A Suprachoroidal Electrical Retinal Stimulator Design for Long-Term Animal Experiments and In Vivo Assessment of Its Feasibility and Biocompatibility in Rabbits , 2008, Journal of biomedicine & biotechnology.

[20]  E. Chichilnisky,et al.  Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. , 2006, Journal of neurophysiology.

[21]  F. Werblin,et al.  A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation. , 2006, Journal of neurophysiology.

[22]  James Weiland,et al.  Neural responses elicited by electrical stimulation of the retina. , 2006, Transactions of the American Ophthalmological Society.

[23]  G. J. Suaning,et al.  Focal activation of the feline retina via a suprachoroidal electrode array , 2009, Vision Research.

[24]  J. Morley,et al.  Visual cortical potentials of the mouse evoked by electrical stimulation of the retina , 2008, Brain Research Bulletin.

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

[26]  Jessy D. Dorn,et al.  Blind subjects implanted with the Argus II retinal prosthesis are able to improve performance in a spatial-motor task , 2010, British Journal of Ophthalmology.

[27]  Richard G. Shiavi,et al.  Wavelet Methods for Spike Detection in Mouse Renal Sympathetic Nerve Activity , 2007, IEEE Transactions on Biomedical Engineering.

[28]  G. V. Wermeskerken,et al.  A comparison of intra- versus post-operatively acquired electrically evoked compound action potentials. , 2006 .

[29]  Michael Bach,et al.  ISCEV standard for clinical visual evoked potentials (2009 update) , 2010, Documenta Ophthalmologica.

[30]  Joseph F Rizzo,et al.  Comparison of electrically evoked cortical potential thresholds generated with subretinal or suprachoroidal placement of a microelectrode array in the rabbit , 2005, Journal of neural engineering.

[31]  Fan-Gang Zeng,et al.  Cochlear Implants: Auditory Prostheses and Electric Hearing , 2004, Springer Handbook of Auditory Research.

[32]  Fan-Gang Zeng,et al.  Auditory Prostheses: Past, Present, and Future , 2004 .

[33]  Liming Li,et al.  Response properties of electrically evoked potential elicited by multi-channel penetrative optic nerve stimulation in rabbits , 2009, Documenta Ophthalmologica.

[34]  Malini Narayanan Nadig Development of a silicon retinal implant: cortical evoked potentials following focal stimulation of the rabbit retina with light and electricity , 1999, Clinical Neurophysiology.

[35]  N. H. Lovell,et al.  Efficacy of supra-choroidal, bipolar, electrical stimulation in a vision prosthesis , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[36]  Thomas Stieglitz,et al.  Chronically implanted epidural electrodes in Göttinger minipigs allow function tests of epiretinal implants , 2003, Graefe's Archive for Clinical and Experimental Ophthalmology.

[37]  James D. Weiland,et al.  1 Visual Prosthesis 2 Microelectronic implants that provide identification of simple objects and motion 3 detection for blind patients have been tested and evaluated; further development is 4 needed for face recognition and reading implants. , 2008 .

[38]  Y. Tano,et al.  Efficacy of suprachoroidal-transretinal stimulation in a rabbit model of retinal degeneration. , 2010, Investigative ophthalmology & visual science.

[39]  Gislin Dagnelie,et al.  Visual perception in a blind subject with a chronic microelectronic retinal prosthesis , 2003, Vision Research.

[40]  R. Jensen,et al.  Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes. , 2005, Investigative ophthalmology & visual science.

[41]  J. Morley,et al.  In vivo evaluation of an episcleral multielectrode array for stimulation of the retina with reduced retinal ganglion cell mass , 2008, Journal of Clinical Neuroscience.

[42]  Guido F. Smoorenburg,et al.  Speech Perception in Nucleus CI24M Cochlear Implant Users with Processor Settings Based on Electrically Evoked Compound Action Potential Thresholds , 2002, Audiology and Neurotology.

[43]  F. Rattay,et al.  The basic mechanism for the electrical stimulation of the nervous system , 1999, Neuroscience.