Electric Stimulation Elicits Heterogeneous Responses in ON but Not OFF Retinal Ganglion Cells to Transmit Rich Neural Information.

Joon Ho Kang,Soo Hyun Lee,Ye Ji Jang,Byung Chul Lee,Taegon Kim,Maesoon Im

doi:10.1109/tnsre.2020.3048973

Abstract

Retinal implants electrically stimulate surviving retinal neurons to restore vision in people blinded by outer retinal degeneration. Although the healthy retina is known to transmit a vast amount of visual information to the brain, it has not been studied whether prosthetic vision contains a similar amount of information. Here, we assessed the neural information transmitted by population responses arising in brisk transient (BT) and brisk sustained (BS) subtypes of ON and OFF retinal ganglion cells (RGCs) in the rabbit retina. To correlate the response heterogeneity and the information transmission, we first quantified the cell-to-cell heterogeneity by calculating the spike time tiling coefficient (STTC) across spiking patterns of RGCs in each type. Then, we computed the neural information encoded by the RGC population in a given type. In responses to light stimulation, spiking activities were more heterogeneous in OFF than ON RGCs (STTCAVG = 0.36, 0.45, 0.77 and 0.55 for OFF BT, OFF BS, ON BT, and ON BS, respectively). Interestingly, however, in responses to electric stimulation, both BT and BS subtypes of OFF RGCs showed remarkably homogeneous spiking patterns across cells (STTCAVG = 0.93 and 0.82 for BT and BS, respectively), whereas the two subtypes of ON RGCs showed slightly increased populational heterogeneity compared to light-evoked responses (STTCAVG = 0.71 and 0.63 for BT and BS, respectively). Consequently, the neural information encoded by the electrically-evoked responses of a population of 15 RGCs was substantially lower in the OFF than the ON pathway: OFF BT and BS cells transmit only ~23% and ~53% of the neural information transmitted by their ON counterparts. Together with previously-reported natural spiking activities in ON RGCs, the higher neural information may make ON responses more recognizable, eliciting the biased percepts of bright phosphenes.

Highlights

T HE goal of microelectronic retinal implants is to restore the vision of blind people by electrically stimulating retinal neurons that survive outer retinal degenerative diseases including retinitis pigmentosa (RP) and age-related macular degeneration (AMD) [1]–[3]
Considering qualitative speculation of heterogeneity from the firing rate heat maps, spiking activities arising from light stimulation seemed largely heterogeneous across retinal ganglion cells (RGCs) in each type (Figs. 2C-2J), while electric stimulation could not conserve this heterogeneity in the OFF types
Since the heterogeneity of spiking patterns correlates with the information encoded in the population response [32]–[37], our results suggest the neural information carried by electric responses of OFF cells is likely to be substantially different from that of ON cells as well as to that of their own light responses

Summary

Introduction

T HE goal of microelectronic retinal implants is to restore the vision of blind people by electrically stimulating retinal neurons that survive outer retinal degenerative diseases including retinitis pigmentosa (RP) and age-related macular degeneration (AMD) [1]–[3]. Various research groups have introduced new designs of microelectrodes [8]–[11] and/or new materials such as nanowires [12] and nanoparticles [13] to further improve the spatial resolution of retinal implants. In addition to those engineering efforts, it is critical to make electrically-elicited neural activities created by retinal implants similar to visually-elicited neural activities created by the healthy retina for improved artificial vision [1], [14], [15]. Given that electric pulse can produce more physiological-like spiking patterns in ON than OFF cells [14], it is likely to make overall retinal responses more natural

Methods

Results

Conclusion