A model of ganglion axon pathways accounts for percepts elicited by retinal implants

Michael Beyeler,Devyani Nanduri,Geoffrey M. Boynton,Ione Fine,Ariel Rokem,James D. Weiland

doi:10.1038/s41598-019-45416-4

Abstract

Degenerative retinal diseases such as retinitis pigmentosa and macular degeneration cause irreversible vision loss in more than 10 million people worldwide. Retinal prostheses, now implanted in over 250 patients worldwide, electrically stimulate surviving cells in order to evoke neuronal responses that are interpreted by the brain as visual percepts (‘phosphenes’). However, instead of seeing focal spots of light, current implant users perceive highly distorted phosphenes that vary in shape both across subjects and electrodes. We characterized these distortions by asking users of the Argus retinal prosthesis system (Second Sight Medical Products Inc.) to draw electrically elicited percepts on a touchscreen. Using ophthalmic fundus imaging and computational modeling, we show that elicited percepts can be accurately predicted by the topographic organization of optic nerve fiber bundles in each subject’s retina, successfully replicating visual percepts ranging from ‘blobs’ to oriented ‘streaks’ and ‘wedges’ depending on the retinal location of the stimulating electrode. This provides the first evidence that activation of passing axon fibers accounts for the rich repertoire of phosphene shape commonly reported in psychophysical experiments, which can severely distort the quality of the generated visual experience. Overall our findings argue for more detailed modeling of biological detail across neural engineering applications.

Highlights

Degenerative retinal diseases such as retinitis pigmentosa[1] and macular degeneration[2] lead to a loss of photoreceptor cells and subsequent remodeling of the neural circuitry in the retina[3,4], causing irreversible blindness in more than 10 million people worldwide
Four subjects suffering from severe retinitis pigmentosa (Table 1) were chronically implanted with an epiretinal prosthesis in the macular region of the retina: one subject was implanted with an Argus I device (16 platinum disc electrodes arranged in a 4x4 checkerboard pattern; see Fig. 1A), and three subjects were implanted with Argus II device (60 platinum disc electrodes in a 6x10 arrangement; Fig. 1B)
Mean images were centered over the corresponding electrode in a schematic of the subject's implant to reveal the rich repertoire of elicited percepts across electrodes

Summary

Introduction

Degenerative retinal diseases such as retinitis pigmentosa[1] and macular degeneration[2] lead to a loss of photoreceptor cells and subsequent remodeling of the neural circuitry in the retina[3,4], causing irreversible blindness in more than 10 million people worldwide. Most subjects cannot determine the orientation of gratings that are used to measure visual acuity, and those who can recognize letters take more than 40 seconds to do so[26,27] Both computational[28,29] and in vitro electrophysiological studies[17,30,31] suggest that electrode configurations similar to those implanted in patients do not achieve focal activation, but rather produce significant activation of passing axon fibers, which may result in perceptual distortions in patients. Our computational model can account for the apparent shape of phosphenes elicited by single-electrode stimulation in two generations of the Argus retinal prosthesis system (Second Sight Medical Products Inc.). The model assumed that distortions are due to activation of ganglion axon pathways, having estimated the spatial layout of these pathways using traced nerve fiber bundle trajectories extracted from ophthalmic fundus photographs of 55 human eyes[32]

Methods

Results

Conclusion