The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

Electrically-evoked Neural Activities of rd1 Mice Retinal Ganglion Cells by Repetitive Pulse Stimulation

  • Ryu, Sang-Baek (Department of Biomedical Engineering, College of Health Science, Yonsei University) ;
  • Ye, Jang-Hee (Department of Physiology, Chungbuk National University School of Medicine) ;
  • Lee, Jong-Seung (Department of Biomedical Engineering, College of Health Science, Yonsei University) ;
  • Goo, Yong-Sook (Department of Physiology, Chungbuk National University School of Medicine) ;
  • Kim, Chi-Hyun (Department of Biomedical Engineering, College of Health Science, Yonsei University) ;
  • Kim, Kyung-Hwan (Department of Biomedical Engineering, College of Health Science, Yonsei University)
  • Published : 2009.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

For successful visual perception by visual prosthesis using electrical stimulation, it is essential to develop an effective stimulation strategy based on understanding of retinal ganglion cell (RGC) responses to electrical stimulation. We studied RGC responses to repetitive electrical stimulation pulses to develop a stimulation strategy using stimulation pulse frequency modulation. Retinal patches of photoreceptor-degenerated retinas from rd1 mice were attached to a planar multi-electrode array (MEA) and RGC spike trains responding to electrical stimulation pulse trains with various pulse frequencies were observed. RGC responses were strongly dependent on inter-pulse interval when it was varied from 500 to 10 ms. Although the evoked spikes were suppressed with increasing pulse rate, the number of evoked spikes were >60% of the maximal responses when the inter-pulse intervals exceeded 100 ms. Based on this, we investigated the modulation of evoked RGC firing rates while increasing the pulse frequency from 1 to 10 pulses per second (or Hz) to deduce the optimal pulse frequency range for modulation of RGC response strength. RGC response strength monotonically and linearly increased within the stimulation frequency of 1~9 Hz. The results suggest that the evoked neural activities of RGCs in degenerated retina can be reliably controlled by pulse frequency modulation, and may be used as a stimulation strategy for visual neural prosthesis.

Keywords

References

  1. Ahuja AK, Behrend MR, Kuroda M, Humayun MS, Weiland JD. An in-vitro model of a retinal implant. IEEE Trans Biomed Eng 55: 1744-1753, 2008 https://doi.org/10.1109/TBME.2008.919126
  2. Fried SI, Hsueh HA, Werblin FS. A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation. J Neurophysiol 95: 970-978, 2006 https://doi.org/10.1152/jn.00849.2005
  3. Hesse L, Schanze T, Wilms M, Eger M. Implantation of retina stimulation electrodes and recording of electrical stimulation responses in the visual cortex of the cat. Graef Arch Clin Exp Ophthal 238: 840-845, 2000 https://doi.org/10.1007/s004170000197
  4. Hornig R, Laube T, Walter P, Velikay-Parel M, Bornfeld N, Feucht M, Akguel H, Rössler G, Alteheld N, Notarp DL, Wyatt J, Richard G. A method and technical equipment for an acute human trial to evaluate retinal implant technology. J Neural Eng 2: S129-S124, 2005 https://doi.org/10.1088/1741-2560/2/1/014
  5. Humayun MS, de Juan E Jr, Weiland JD, Dangnelie G, Katona S, Greenberg R, Suzuki S. Pattern electrical stimulation of the human retina. Vision Res 39: 2569-2576, 1999 https://doi.org/10.1016/S0042-6989(99)00052-8
  6. Humayun MS, Weiland JD, Fujii GY, Greenberg R, Williamson R, Little J, Mech B, Cimmarusti V, Boemel GV, Dagnelie G, de Juan E Jr. Visual perception in a blind subject with a chronic microelectronic retinal prosthesis. Vision Res 43: 2573-2581, 2003 https://doi.org/10.1016/S0042-6989(03)00457-7
  7. Jensen RJ, Rizzo JF III. Responses of ganglion cells to repetitive electrical stimulation of the retina. J Neural Eng 4: S1-S6, 2007 https://doi.org/10.1088/1741-2560/4/1/S01
  8. Jensen RJ, Ziv OR, Rizzo JF. Responses of rabbit retinal ganglion cells to electrical stimulation with an epiretinal electrode. J Neural Eng 2: S16-S21, 2005 https://doi.org/10.1088/1741-2560/2/1/003
  9. Kazemi M, Basham E, Sivaprakasam M, Wang G, Rodger D, Weiland J, Tai YC, Liu W, Humayun M. A test microchip for evaluation of hermetic packaging technology for biomedical prosthetic implants. Conf Proc IEEE Eng Med Biol Soc 6: 4093-4095, 2004
  10. Margolis DJ, Newkirk G, Euler T, Detwiler PB. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci 28: 6526-6536, 2008 https://doi.org/10.1523/JNEUROSCI.1533-08.2008
  11. Merabet LB, Rizzo JF, Amedi A, Somers DC, Pascual-Leone A. What blindness can tell us about seeing again: merging neuroplasticity and neuroprosthesis. Nat Rev Neurosci 6: 71-77, 2005 https://doi.org/10.1038/nrn1586
  12. Rizzo JF III, Wyatt J, Loewenstein J, Kelly S, Shire D. Perceptual efficacy of electrical stimulation of human retina with a microelectrode array during short-term surgical trials. Invest Ophth Vis Sci 44: 5362-5369, 2003 https://doi.org/10.1167/iovs.02-0817
  13. Ryu SB, Lee JS, Ye JH, Goo YS, Kim CH, Kim KH. Analysis of neuronal activities of retinal ganglion cells of degenerated retinal evoked by electrical pulse stimulation. J Biomed Eng Res 30: 347-354, 2009a
  14. Ryu SB, Ye JH, Lee JS, Goo YS, Kim KH. Characterization of retinal ganglion cell activities evoked by temporally patterned electrical stimulation for the development of stimulus encoding strategies for retinal implants. Brain Res 1275: 33-42, 2009b https://doi.org/10.1016/j.brainres.2009.03.064
  15. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ. Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. J Neurophysiol 95: 3311-3327, 2006 https://doi.org/10.1152/jn.01168.2005
  16. Seo JM, Kim SJ, Chung H, Kim ET, Yu HG, Yu YS. Biocompatibility of polyimide microelectrode array for retinal stimulation. Mater Sci Eng C 24: 185-189, 2004 https://doi.org/10.1016/j.msec.2003.09.019
  17. Sivaprakasam M, Wentai L, Guoxing W, Weiland JD, Humayun MS. Architecture tradeoffs in high-density microstimulators for retinal prosthesis. IEEE Trans Circuits Syst I-Regul Pap 52: 2629-2641, 2005 https://doi.org/10.1109/TCSI.2005.857554
  18. Stasheff SF. Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J Neurophysiol 99: 1408-1421, 2008 https://doi.org/10.1152/jn.00144.2007
  19. Stett A, Barth W, Weiss S, Haemmerle H, Zrenner E. Electrical multisite stimulation of the isolated chicken retina. Vis Res 40: 1785-1795, 2000 https://doi.org/10.1016/S0042-6989(00)00005-5
  20. Veraart C, Raftopoulos C, Mortmer JT, Delbeke J, Pins D, Michaus G, Vanlierde A, Parrini S, Wanet-Defalqu M. Visual sensations produced by optic nerve stimulation using an implanted self-sizing spiral cuff electrode. Brain Res 813: 181-186, 1998 https://doi.org/10.1016/S0006-8993(98)00977-9
  21. Ye JH, Goo YS. The slow wave component of retinal activity in rd/rd mouse recorded with a multi-electrode array. Physiol Meas 28: 1079-1088, 2007 https://doi.org/10.1088/0967-3334/28/9/009
  22. Zrenner E. Will retinal implants restore vision? Science 295: 1022-1025, 2002 https://doi.org/10.1126/science.1067996

Cited by

  1. Retinal ganglion cell responses to voltage and current stimulation in wild-type and rd1 mouse retinas vol.8, pp.3, 2009, https://doi.org/10.1088/1741-2560/8/3/035003
  2. Encoding visual information in retinal ganglion cells with prosthetic stimulation vol.8, pp.3, 2011, https://doi.org/10.1088/1741-2560/8/3/035005
  3. Topographic prominence discriminator for the detection of short-latency spikes of retinal ganglion cells vol.14, pp.1, 2017, https://doi.org/10.1088/1741-2552/aa5646
  4. Spike-triggered average electrical stimuli as input filters for bionic vision—a perspective vol.15, pp.6, 2009, https://doi.org/10.1088/1741-2552/aae493