Restoring Color Perception to the Blind

An Electrical Stimulation Strategy of Retina in Patients with End-stage Retinitis Pigmentosa

      Purpose

      Bioelectronic retinal prostheses that stimulate the remaining inner retinal neurons, bypassing degenerated photoreceptors, have been demonstrated to restore some vision in patients blinded by retinitis pigmentosa (RP). These implants encode luminance of the visual scene into electrical stimulation, however, leaving out chromatic information. Yet color plays an important role in visual processing when it comes to recognizing objects and orienting to the environment, especially at low spatial resolution as generated by current retinal prostheses. In this study, we tested the feasibility of partially restoring color perception in blind RP patients, with the aim to provide chromatic information as an extra visual cue.

      Design

      Case series.

      Participants

      Seven subjects blinded by advanced RP and monocularly fitted with an epiretinal prosthesis.

      Methods

      Frequency-modulated electrical stimulation of retina was tested. Phosphene brightness was controlled by amplitude tuning, and color perception was acquired using the Red, Yellow, Green, and Blue (RYGB) hue and saturation scaling model.

      Main Outcome Measures

      Brightness and color of the electrically elicited visual perception reported by the subjects.

      Results

      Within the tested parameter space, 5 of 7 subjects perceived chromatic colors along or nearby the blue-yellow axis in color space. Aggregate data obtained from 20 electrodes of the 5 subjects show that an increase of the stimulation frequency from 6 to 120 Hz shifted color perception toward blue/purple despite a significant inter-subject variation in the transition frequency. The correlation between frequency and blue-yellow perception exhibited a good level of consistency over time and spatially matched multi-color perception was possible with simultaneous stimulation of paired electrodes. No obvious correlation was found between blue sensations and array placement or status of visual impairment.

      Conclusions

      These findings present a strategy for the generation and control of color perception along the blue-yellow axis in blind patients with RP by electrically stimulating the retina. It could transform the current prosthetic vision landscape by leading in a new direction beyond the efforts to improve the visual acuity. This study also offers new insights into the response of our visual system to electrical stimuli in the photoreceptor-less retina that warrant further mechanistic investigation.

      Keywords

      Abbreviations and Acronyms:

      F (frequency), PW (pulse width), RGC (retinal ganglion cell), RP (retinitis pigmentosa), RYGB (Red, Yellow, Green, and Blue)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic and Personal

      Subscribe:

      Subscribe to Ophthalmology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bramão I.
        • Faísca L.
        • Petersson K.M.
        • Reis A.
        The Contribution of Color to Object Recognition.
        in: Kypraios I. Advances in object recognition systems. InTech, Rijeka, Croatia2012: 73-88 (Available at: http://www.intechopen.com/books/advances-in-object-recognition-systems/the-contribution-of-color-in-object-recognition)
        • Tanaka J.
        • Weiskopf D.
        • Williams P.
        The role of color in high-level vision.
        Trends Cogn Sci. 2001; 5: 211-215
        • Rossion B.
        • Pourtois G.
        Revisiting Snodgrass and Vanderwart's object pictorial set: the role of surface detail in basic-level object recognition.
        Perception. 2004; 33: 217-236
        • Uttl B.
        • Graf P.
        • Santacruz P.
        Object color affects identification and repetition priming.
        Scand J Psychol. 2006; 47: 313-325
        • Nathans J.
        The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments.
        Neuron. 1999; 24: 299-312
        • Dacey D.M.
        Circuitry for color coding in the primate retina.
        Proc Natl Acad Sci. 1996; 93: 582-588
        • Bressler N.M.
        Age-related macular degeneration is the leading cause of blindness.
        JAMA. 2004; 291: 1900-1901
        • den Hollander A.I.
        • ten Brink J.B.
        • de Kok Y.J.
        • et al.
        Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12).
        Nat Genet. 1999; 23: 217-221
        • Jackson G.R.
        • Owsley C.
        • Curcio C.A.
        Photoreceptor degeneration and dysfunction in aging and age-related maculopathy.
        Ageing Res Rev. 2002; 1: 381-396
        • Hartong D.T.
        • Berson E.L.
        • Dryja T.P.
        Retinitis pigmentosa.
        Lancet. 2006; 368: 1795-1809
        • Stanga P.
        • Jalil A.
        • Tsamis E.
        • et al.
        Argus II® Electronic Epiretinal Prosthesis in Advanced Dry AMD: Safety and Feasibility Study and Preliminary Functional Results.
        ARVO, Seattle, WA2016
        • Stingl K.
        • Bartz-Schmidt K.U.
        • Besch D.
        • et al.
        Subretinal visual implant alpha IMS–clinical trial interim report.
        Vision Res. 2015; 111: 149-160
        • Yue L.
        • Weiland J.D.
        • Roska B.
        • Humayun M.S.
        Retinal stimulation strategies to restore vision: Fundamentals and systems.
        Prog Retin Eye Res. 2016; 53: 21-47
        • Stanga P.
        • Hafezi F.
        • Sahel J.
        • et al.
        Patients blinded by outer retinal dystrophies are able to perceive color using the Argus II Retinal Prosthesis System.
        ARVO. 2011; 2011: 1-5
        • Hornig R.
        • Zehnder T.
        • Velikay-Parel M.
        • et al.
        The IMI retinal implant system.
        Artificial Sight. Springer, New York2007: 111-128
        • Stanga P.E.
        • Sahel Jr., J.A.
        • Hafezi F.
        • et al.
        Patients blinded by outer retinal dystrophies are able to perceive simultaneous colors using the Argus® II retinal prosthesis system.
        Invest Ophthalmol Vis Sci. 2012; 53 (6952-6952)
        • Gordon J.
        • Abramov I.
        • Chan H.
        Describing color appearance: hue and saturation scaling.
        Percept Psychophys. 1994; 56: 27-41
      1. Dacey DM. Physiology, morphology and spatial densities of identified ganglion cell. Paper presented at: Symposium on Higher-order processing in the visual system, held at the Ciba Foundation, London, 19-21, October 1993.

        • Neitz J.
        • Neitz M.
        Evolution of the circuitry for conscious color vision in primates.
        Eye. 2017; 31: 286
        • Neitz J.
        • Neitz M.
        The genetics of normal and defective color vision.
        Vision Res. 2011; 51: 633-651
        • Jensen R.J.
        • Rizzo III, J.F.
        Responses of ganglion cells to repetitive electrical stimulation of the retina.
        J Neural Eng. 2007; 4: S1
        • Freeman D.K.
        • Fried S.I.
        Multiple components of ganglion cell desensitization in response to prosthetic stimulation.
        J Neural Eng. 2011; 8016008
        • Ahuja A.K.
        • Behrend M.R.
        • Kuroda M.
        • et al.
        An in vitro model of a retinal prosthesis.
        IEEE Trans Biomed Eng. 2008; 55: 1744-1753
        • Stronks H.C.
        • Dagnelie G.
        The functional performance of the Argus II retinal prosthesis.
        Expert Rev Med Devices. 2014; 11: 23-30
        • Hadjinicolaou A.
        • Savage C.
        • Apollo N.
        • et al.
        Optimizing the electrical stimulation of retinal ganglion cells.
        IEEE Trans Neural Syst Rehabil Eng. 2014; 23: 169-178
        • Cai C.
        • Ren Q.
        • Desai N.J.
        • et al.
        Response variability to high rates of electric stimulation in retinal ganglion cells.
        J Neurophysiol. 2011; 106: 153-162
        • Fried S.I.
        • Hsueh H.-A.
        • Werblin F.S.
        A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation.
        J Neurophysiol. 2006; 95: 970-978
        • McCreery D.
        Tissue reaction to electrodes: The problem of safe and effective stimulation of neural tissue.
        in: Neuroprosthetics: Theory and Practice. World Scientific, Singapore2004: 592-611
        • Cohen E.
        • Agrawal A.
        • Connors M.
        • et al.
        Optical coherence tomography imaging of retinal damage in real time under a stimulus electrode.
        J Neural Eng. 2011; 8056017