Decoding of Temporal Visual Information from Electrically Evoked Retinal Ganglion Cell Activities in Photoreceptor-Degenerated Retinas

Abstract

PURPOSE.To restore visual function via the prosthetic stimulation of retina, visual information must be properly represented in the electrically evoked neural activity of retinal ganglion cells (RGCs). In this study, the RGC responses in photoreceptor-degenerated retinas were shown to actually encode temporal information on visual input when they were stimulated by biphasic pulse trains with amplitude modulation. METHODS. Multiple RGC spike trains were recorded from rd1 mouse retinal patches mounted on planar microelectrode arrays while being stimulated by pulse trains with amplitudes modulated by the intensity variation of a natural scene. To reconstruct the time series of pulse train amplitudes from the evoked RGC activity, spike train decoding was performed. The accuracy of decoding-that is, the similarity between the original and decoded pulse amplitudes-was observed, to evaluate the appropriateness of the stimulation. RESULTS. The response strengths of the RGCs could be successfully modulated when the pulse amplitude was varied between 2 and 20 A. When the amplitude modulation range and pulse rates were determined elaborately, the temporal profile of the intensity could be successfully decoded from RGC spike trains, although abnormal oscillatory background rhythms (ϳ10 Hz) were consistently present in the rd1 spike activity. CONCLUSIONS. The results extend previous findings on the possibility of visual information encoding by electrical stimulation of normal retinas to stimulate degenerated retinas, in which neural activity is significantly altered. This supports the feasibility of encoding of temporal information by retinal prostheses. (Invest Ophthalmol Vis Sci. 2011;52:6271-6278 For the successful restoration of visual function, neural responses evoked by electrical stimulation should accurately represent spatiotemporal information on visual input. We have recently shown that in the normal retina, this is feasible through amplitude modulation of pulse trains when the parameters of stimulation are carefully selected.9,10 However, it has been recognized that RGC activity is significantly altered in the degenerated retina due to changes in synaptic properties 11,12 ; thus, abnormal rhythmic oscillation is present in both spontaneous and stimulated neural activity. Because this rhythmic oscillation does not originate from external visual inputs, it may disturb the representation and transmission of visual information by RGC activity in blind persons. Thus, visual information encoded by prosthetic electrical stimulation should be observed carefully in the degenerated retina.Quantitative investigation into information encoding by neuronal networks can be performed by spike train decoding, which consists of estimating (decoding) quantitative information encoded in neuronal activity. Typical applications include the study of fundamental visual information encoding characteristics of neuronal populations 13,14 and the control of brain-machine interfaces. 15 In the present study, we sought to determine whether it ...

High-Fidelity Reproduction of Spatiotemporal Visual Signals for Retinal Prosthesis

“…Although the combination of cell-type specificity, spatial and temporal precision, and completeness of electrically elicited activity exceeded the scope of previous work (Nirenberg and Pandarinath, 2012; Jensen et al, 2009; Hottowy et al, 2012; Fried et al, 2006; Ryu et al, 2011), additional work would be required to fully understand the generality and impact of these findings for future epiretinal prostheses, for several reasons.

Although focal activation of individual cells is clearly possible among the dominant RGC types in the primate retina (Sekirnjak et al, 2008; Jepson et al, 2013), and was achieved here in small collections of ON parasol cells, the reliability of activation of one cell without activation of any cells of other types has yet to be fully documented.

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“…Although present-day prostheses produce only limited visual function (Dorn et al, 2013; G. Richard et al, 2008, ARVO abstract; Klauke et al, 2011; Barry and Dagnelie, 2012; Humayun et al, 2012; da Cruz et al, 2013), experiments in isolated retina have demonstrated the capacity to electrically stimulate individual retinal ganglion cells (RGCs) to fire individual spikes (Jensen et al, 2005; Fried et al, 2006) with high spatial and temporal precision (Fried et al, 2006; Sekirnjak et al, 2006; Sekirnjak et al, 2008; Hottowy et al, 2012; Jepson et al, 2013). These findings raise the possibility of faithful reproduction of the neural code of the retina, and thus much more acute artificial vision, with future prostheses (see Jensen et al, 2009; Fried et al, 2006; Ryu et al, 2011). However, it is well known that naturalistic visual experience relies not on the activity of any individual RGC but on diverse spatiotemporal patterns of activity in multiple distinct populations of RGCs.…”

Amplitude Modulation-based Electrical Stimulation for Encoding Multipixel Spatiotemporal Visual Information in Retinal Neural Activities

“…In our recent studies on temporal information encoding by electrically stimulated RGCs, the pulse amplitude time-series could be successfully reconstructed from evoked RGC activities (67). This is supported by recent reports on human clinical trials of retinal implants, such as the report of Greenwald et al (18), where it was shown that the brightness of the phosphene elicited by electrical stimulation of the retina followed the current amplitude.…”

“…The overall procedure for spike train decoding is illustrated in detail in Fig. 2 of Ryu et al (7) and briefly described herein. The raw waveforms from each electrode were transformed into single unit spike trains, and then, the RGC spike trains were transformed to a firing rate time-series by counting the numbers of spikes in 50 ms bins.…”

“…We have recently shown that temporal patterns of visual input could be successfully decoded from population activities of RGCs evoked by a temporally patterned stimulation pulse train, in both normal (6) and photoreceptor-degenerated retinas (7). Cottaris and Elfar (8) demonstrated that the spatial origin, duration, and amplitude of each stimulation pulse could be identified with multisite cortical local field potential.…”