DOI QR코드

DOI QR Code

The advantage of topographic prominence-adopted filter for the detection of short-latency spikes of retinal ganglion cells

  • Ahn, Jungryul (Department of Physiology, Chungbuk National University School of Medicine) ;
  • Choi, Myoung-Hwan (Department of Biomedical Engineering, University of Ulsan) ;
  • Kim, Kwangsoo (Department of Electronics and Control Engineering, Hanbat National University) ;
  • Senok, Solomon S. (Ajman University School of Medicine) ;
  • Cho, Dong-il Dan (Department of Electrical and Computer Engineering, Seoul National University) ;
  • Koo, Kyo-in (Department of Biomedical Engineering, University of Ulsan) ;
  • Goo, Yongsook (Department of Physiology, Chungbuk National University School of Medicine)
  • Received : 2017.07.11
  • Accepted : 2017.08.03
  • Published : 2017.09.01

Abstract

Electrical stimulation through retinal prosthesis elicits both short and long-latency retinal ganglion cell (RGC) spikes. Because the short-latency RGC spike is usually obscured by electrical stimulus artifact, it is very important to isolate spike from stimulus artifact. Previously, we showed that topographic prominence (TP) discriminator based algorithm is valid and useful for artifact subtraction. In this study, we compared the performance of forward backward (FB) filter only vs. TP-adopted FB filter for artifact subtraction. From the extracted retinae of rd1 mice, we recorded RGC spikes with $8{\times}8$ multielectrode array (MEA). The recorded signals were classified into four groups by distances between the stimulation and recording electrodes on MEA (200-400, 400-600, 600-800, $800-1000{\mu}m$). Fifty cathodic phase-$1^{st}$ biphasic current pulses (duration $500{\mu}s$, intensity 5, 10, 20, 30, 40, 50, $60{\mu}A$) were applied at every 1 sec. We compared false positive error and false negative error in FB filter and TP-adopted FB filter. By implementing TP-adopted FB filter, short-latency spike can be detected better regarding sensitivity and specificity for detecting spikes regardless of the strength of stimulus and the distance between stimulus and recording electrodes.

Keywords

References

  1. Shintani K, Shechtman DL, Gurwood AS. Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry. 2009;80:384-401. https://doi.org/10.1016/j.optm.2008.01.026
  2. Mehta S. Age-related macular degeneration. Prim Care. 2015;42:377-391. https://doi.org/10.1016/j.pop.2015.05.009
  3. Kim SY, Sadda S, Pearlman J, Humayun MS, de Juan E Jr, Melia BM, Green WR. Morphometric analysis of the macula in eyes with disciform age-related macular degeneration. Retina. 2002;22:471-477. https://doi.org/10.1097/00006982-200208000-00012
  4. Mazzoni F, Novelli E, Strettoi E. Retinal ganglion cells survive and maintain normal dendritic morphology in a mouse model of inherited photoreceptor degeneration. J Neurosci. 2008;28:14282-14292. https://doi.org/10.1523/JNEUROSCI.4968-08.2008
  5. Santos A, Humayun MS, de Juan E Jr, Greenburg RJ, Marsh MJ, Klock IB, Milam AH. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch Ophthalmol. 1997; 115:511-515. https://doi.org/10.1001/archopht.1997.01100150513011
  6. Stone JL, Barlow WE, Humayun MS, de Juan E Jr, Milam AH. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch Ophthalmol. 1992;110:1634-1639. https://doi.org/10.1001/archopht.1992.01080230134038
  7. Stingl K, Bartz-Schmidt KU, Besch D, Chee CK, Cottriall CL, Gekeler F, Groppe M, Jackson TL, MacLaren RE, Koitschev A, Kusnyerik A, Neffendorf J, Nemeth J, Naeem MA, Peters T, Ramsden JD, Sachs H, Simpson A, Singh MS, Wilhelm B, Wong D, Zrenner E. Subretinal visual implant alpha IMS-clinical trial interim report. Vision Res. 2015;111:149-160. https://doi.org/10.1016/j.visres.2015.03.001
  8. Luo YH, da Cruz L. The $argus^{(R)}$ II retinal prosthesis system. Prog Retin Eye Res. 2016;50:89-107. https://doi.org/10.1016/j.preteyeres.2015.09.003
  9. Ahn KN, Ahn JY, Kim JH, Cho K, Koo KI, Senok SS, Goo YS. Effect of stimulus waveform of biphasic current pulse on retinal ganglion cell responses in retinal degeneration (rd1) mice. Korean J Physiol Pharmacol. 2015;19:167-175. https://doi.org/10.4196/kjpp.2015.19.2.167
  10. Boinagrov D, Pangratz-Fuehrer S, Goetz G, Palanker D. Selectivity of direct and network-mediated stimulation of the retinal ganglion cells with epi-, sub- and intraretinal electrodes. J Neural Eng. 2014;11:026008. https://doi.org/10.1088/1741-2560/11/2/026008
  11. Jensen RJ, Ziv OR, Rizzo JF 3rd. Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes. Invest Ophthalmol Vis Sci. 2005;46:1486-1496. https://doi.org/10.1167/iovs.04-1018
  12. Lee SW, Eddington DK, Fried SI. Responses to pulsatile subretinal electric stimulation: effects of amplitude and duration. J Neurophysiol. 2013;109:1954-1968. https://doi.org/10.1152/jn.00293.2012
  13. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ. Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. J Neurophysiol. 2006;95:3311-3327. https://doi.org/10.1152/jn.01168.2005
  14. Stett A, Barth W, Weiss S, Haemmerle H, Zrenner E. Electrical multisite stimulation of the isolated chicken retina. Vision Res. 2000;40:1785-1795. https://doi.org/10.1016/S0042-6989(00)00005-5
  15. Im M, Fried SI. Indirect activation elicits strong correlations between light and electrical responses in ON but not OFF retinal ganglion cells. J Physiol. 2015;593:3577-3596. https://doi.org/10.1113/JP270606
  16. Grumet AE. Electric stimulation parameters for an epi-retinal prosthesis. (dissertation) Department of Electrical Engineering and Computer Science, Cambridge, MA: Massachusetts Institute of Technology. 1999.
  17. Nagel JH. Biopotential amplifiers. In: Bronzino JD, editor. The biomedical engineering handbook. Boca Raton: CRC Press; 1995. p.1185-1195.
  18. Fried SI, Hsueh HA, Werblin FS. A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation. J Neurophysiol. 2006;95:970-978. https://doi.org/10.1152/jn.00849.2005
  19. Ryu SB, Ye JH, Lee JS, Goo YS, Kim CH, Kim KH. Electricallyevoked neural activities of rd1 mice retinal ganglion cells by repetitive pulse stimulation. Korean J Physiol Pharmacol. 2009;13:443-448. https://doi.org/10.4196/kjpp.2009.13.6.443
  20. Miller CA, Abbas PJ, Robinson BK, Rubinstein JT, Matsuoka AJ. Electrically evoked single-fiber action potentials from cat: responses to monopolar, monophasic stimulation. Hear Res. 1999;130:197-218. https://doi.org/10.1016/S0378-5955(99)00012-X
  21. Heffer LF, Fallon JB. A novel stimulus artifact removal technique for high-rate electrical stimulation. J Neurosci Methods. 2008;170:277-284. https://doi.org/10.1016/j.jneumeth.2008.01.023
  22. Erickson JC, Velasco-Castedo R, Obioha C, Cheng LK, Angeli TR, O'Grady G. Automated algorithm for GI spike burst detection and demonstration of efficacy in ischemic small intestine. Ann Biomed Eng. 2013;41:2215-2228. https://doi.org/10.1007/s10439-013-0812-8
  23. Killian NJ, Vernekar VN, Potter SM, Vukasinovic J. A device for long-term perfusion, imaging, and electrical interfacing of brain tissue in vitro. Front Neurosci. 2016;10:135.
  24. Pan L, Alagapan S, Franca E, Leondopulos SS, DeMarse TB, Brewer GJ, Wheeler BC. An in vitro method to manipulate the direction and functional strength between neural populations. Front Neural Circuits. 2015;9:32.
  25. Choi MH, Ahn J, Park DJ, Lee SM, Kim K, Cho DD, Senok SS, Koo KI, Goo YS. Topographic prominence discriminator for the detection of short-latency spikes of retinal ganglion cells. J Neural Eng. 2017;14:016017. https://doi.org/10.1088/1741-2552/aa5646
  26. Llobera M. Building past landscape perception with GIS: understanding topographic prominence. J Archaeol Sci. 2001;28:1005-1014. https://doi.org/10.1006/jasc.2001.0720
  27. Bullock TH, Horridge AG. Structure and function in the nervous systems of invertebrates. San Francisco, London: W. H. Freeman & Co.; 1965.
  28. Wagenaar DA, Potter SM. Real-time multi-channel stimulus artifact suppression by local curve fitting. J Neurosci Methods. 2002;120:113-120. https://doi.org/10.1016/S0165-0270(02)00149-8
  29. Fawcett T. An introduction to ROC analysis. Pattern Recognit Lett. 2006;27:861-874. https://doi.org/10.1016/j.patrec.2005.10.010
  30. Kuffler SW. Discharge patterns and functional organization of mammalian retina. J Neurophysiol. 1953;16:37-68. https://doi.org/10.1152/jn.1953.16.1.37
  31. Margolis DJ, Newkirk G, Euler T, Detwiler PB. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci. 2008;28:6526-6536. https://doi.org/10.1523/JNEUROSCI.1533-08.2008
  32. Li L, Hayashida Y, Yagi T. Temporal properties of retinal ganglion cell responses to local transretinal current stimuli in the frog retina. Vision Res. 2005;45:263-273. https://doi.org/10.1016/j.visres.2004.08.002
  33. Lu Y, Cao P, Sun J, Wang J, Li L, Ren Q, Chen Y, Chai X. Using independent component analysis to remove artifacts in visual cortex responses elicited by electrical stimulation of the optic nerve. J Neural Eng. 2012;9:026002. https://doi.org/10.1088/1741-2560/9/2/026002