Electrical receptive fields of retinal ganglion cells: Influence of presynaptic neurons

Matias I. Maturana, Nicholas V. Apollo, David J. Garrett, Tatiana Kameneva, Shaun L. Cloherty, David B. Grayden, Anthony N. Burkitt, Michael R. Ibbotson, Hamish Meffin

Research output: Contribution to journalArticleResearchpeer-review

7 Citations (Scopus)

Abstract

Implantable retinal stimulators activate surviving neurons to restore a sense of vision in people who have lost their photoreceptors through degenerative diseases. Complex spatial and temporal interactions occur in the retina during multi-electrode stimulation. Due to these complexities, most existing implants activate only a few electrodes at a time, limiting the repertoire of available stimulation patterns. Measuring the spatiotemporal interactions between electrodes and retinal cells, and incorporating them into a model may lead to improved stimulation algorithms that exploit the interactions. Here, we present a computational model that accurately predicts both the spatial and temporal nonlinear interactions of multi-electrode stimulation of rat retinal ganglion cells (RGCs). The model was verified using in vitro recordings of ON, OFF, and ON-OFF RGCs in response to subretinal multi-electrode stimulation with biphasic pulses at three stimulation frequencies (10, 20, 30 Hz). The model gives an estimate of each cell’s spatiotemporal electrical receptive fields (ERFs); i.e., the pattern of stimulation leading to excitation or suppression in the neuron. All cells had excitatory ERFs and many also had suppressive sub-regions of their ERFs. We show that the nonlinearities in observed responses arise largely from activation of presynaptic interneurons. When synaptic transmission was blocked, the number of sub-regions of the ERF was reduced, usually to a single excitatory ERF. This suggests that direct cell activation can be modeled accurately by a one-dimensional model with linear interactions between electrodes, whereas indirect stimulation due to summated presynaptic responses is nonlinear.

Original languageEnglish
Article numbere1005997
Number of pages31
JournalPLoS Computational Biology
Volume14
Issue number2
DOIs
Publication statusPublished - 12 Feb 2018

Keywords

  • functional electrical stimulation
  • action potentials
  • retinal ganglion cells
  • neurons
  • retina
  • eigenvalues
  • electrode recording
  • visible light

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