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Visual resolution with epi-retinal electrical stimulation estimated from activation profiles in cat visual cortex

Published online by Cambridge University Press:  22 January 2004

MARCUS WILMS ,
MARCUS EGER ,
THOMAS SCHANZE  and
REINHARD ECKHORN[dagger]
MARCUS WILMS
Affiliation:
Institute of Neurophysics, Philipps–University Marburg, 35032 Marburg, Germany
MARCUS EGER
Affiliation:
Institute of Neurophysics, Philipps–University Marburg, 35032 Marburg, Germany
THOMAS SCHANZE
Affiliation:
Institute of Neurophysics, Philipps–University Marburg, 35032 Marburg, Germany
REINHARD ECKHORN[dagger]
Affiliation:
Institute of Neurophysics, Philipps–University Marburg, 35032 Marburg, Germany
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Abstract

Blinds with receptor degeneration can perceive localized phosphenes in response to focal electrical epi-retinal stimuli. To avoid extensive basic stimulation tests in human patients, we developed techniques for estimating visual spatial resolution in anesthetized cats. Electrical epi-retinal and visual stimulation was combined with multiple-site retinal and cortical microelectrode recordings of local field potentials (LFPs) from visual areas 17 and 18. Classical visual receptive fields were characterized for retinal and cortical recording sites using multifocal visual stimulation combined with stimulus–response cross-correlation. We estimated visual spatial resolution from the size of the cortical activation profiles in response to single focal stimuli. For comparison, we determined activation profiles in response to visual stimuli at the same retinal location. Activation profiles were single peaked or multipeaked. In multipeaked profiles, the peak locations coincided with discontinuities in cortical retinotopy. Location and width of cortical activation profiles were distinct for retinal stimulation sites. On average, the activation profiles had a size of 1.28 ± 0.03 mm cortex. Projected to visual space this corresponds to a spatial resolution of 1.49 deg ± 0.04 deg visual angle. Best resolutions were 0.5 deg at low and medium stimulation currents corresponding to a visus of 1/30. Higher stimulation currents caused lower spatial, but higher temporal resolution (up to 70 stimuli/s). In analogy to the receptive-field concept in visual space, we defined and characterized electrical receptive fields. As our estimates of visual resolutions are conservative, we assume that a visual prosthesis will induce phosphenes at least at this resolution. This would enable visuomotor coordinations and object recognition in many indoor and outdoor situations of daily life.

Keywords

Electrical retina stimulationVisual cortexVisual resolutionRetina implant
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 5 , September 2003 , pp. 543 - 555
Copyright
2003 Cambridge University Press

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References

REFERENCES

Anderson, P.A., Olavarria, J., & Van Sluyters, R.C. (1988). The overall pattern of ocular dominance bands in cat visual cortex. Journal of Neuroscience 8, 2183–2200.Google Scholar
Brindley, G.S. & Lewin, W.S. (1968). The sensations produced by electrical stimulation of the visual cortex. Journal of Physiology 196, 479–493.CrossRefGoogle Scholar
Cha, K., Horch, K.W., & Normann, R.A. (1992a). Mobility performance with a pixelized vision system. Vision Research 32.7, 1367–1372.Google Scholar
Cha, K., Horch, K.W., Normann, R.A., & Boman, D. (1992b). Reading speed with a pixelized vision system. Journal of the Optical Society of America A 9.5, 673–677.Google Scholar
Cynader, M., Swindale, N., & Matsubara, J. (1987). Functional topography of cat area 18. Journal of Neuroscience 7.5, 1401–1413.Google Scholar
Dawson, W.W. & Radtke, N.D. (1977). The electrical stimulation of the retina by indwelling electrodes. Investigative Ophthalmology and Visual Science 16.3, 249–252.Google Scholar
Dinse, H. & Krüger, K. (1994). The timing of processing along the visual pathway in the cat. Neuroreport 5, 893–897.CrossRefGoogle Scholar
Dinse, H., Godde, B., Hilger, T., Haupt, S., Spengler, F., & Zepka, R. (1997). Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing. Brain Plasticity 73, 159–178.Google Scholar
Dobelle, W.H. (2000). Artificial vision for the blind by connecting a television camera to the visual cortex. American Society of Artificial and Internal Organs 46, 3–9.CrossRefGoogle Scholar
Dobelle, W.H., Mladejovsky, M.G., & Girvin, J.P. (1974). Artificial vision for the blind: Electrical stimulation of visual cortex offers hope for a functional prosthesis. Science 183, 440–444.CrossRefGoogle Scholar
Eckhorn, R. & Thomas, U. (1993). A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors. Journal of Neuoscience Methods 49, 175–179.Google Scholar
Eckmiller, R. (1997). Learning retina implants with epiretinal contacts. Ophthalmic Research 29, 281–289.CrossRefGoogle Scholar
Eger, M. (2001). Information theoretical methods for the functional adjustment of retina implant parameters. Ph.D. Thesis, Philipps University Marburg.
Ferster, D. & LeVay, S. (1978). The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat. Journal of Comparative Neurology 182, 923–944.CrossRefGoogle Scholar
Fregnac, Y., Bringuier, V., & Chavane, F. (1996). Synaptic integration fields and associative plasticity of visual cortical cells in vivo. Journal of Physiology (Paris) 90, 367–372.CrossRefGoogle Scholar
Gray, C.M., Maldonado, P.E., Wilson, M., & McNaughton, B. (1995). Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. Journal of Neuroscience Methods 63, 43–54.CrossRefGoogle Scholar
Gilbert, C.D. (1993). Circuitry, architecture, and functional dynamics of visual cortex. Cerebral Cortex 3, 373–386.CrossRefGoogle Scholar
Grinvald, A., Lieke, E., Frostig, & R., Hildesheim R. (1994). Cortical point spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. Journal of Neuroscience 14, 2545–2568.Google Scholar
Grüsser, O.-J. & Creutzfeld, O. (1957). Eine neurophysiologische Grundlage des Brücke-Bartley-Effektes: Maxima der Impulsfrequenz retinaler und corticaler Neurone bei Flimmer-Licht mittlerer Frequenzen. Pflügers Archiv der gesamten Physiologie 263, 668–681.CrossRefGoogle Scholar
Hesse, L., Schanze, T., Wilms, M., & Eger, M. (2000). Implantation of retina stimulation electrodes and recording of electrical stimulation responses in the visual cortex of the cat. Graefe's Archive of Clinical and Experimental Ophthalmology 238, 840–845.CrossRefGoogle Scholar
Horton, J. & Hubel, D. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.CrossRefGoogle Scholar
Hubel, D. & Wiesel, T. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle Scholar
Humayun, M.S., Probst, R.H., Juan, E. de, McCormick, K., & Hickingbotham, D. (1994). Bipolar surface electrical stimulation of the vertebrate retina. Archive Ophthalmology 112, 110–116.CrossRefGoogle Scholar
Humayun, M.S., Juan, E. de, Dagnelie, G., Greenberg, R.J., Probst, R.H., & Phillips, D.H. (1996). Visual perception elicited by electrical stimulation of retina in blind humans. Archive Ophthalmology 114, 40–46.CrossRefGoogle Scholar
Humayun, M.S., Juan, E. de, Weiland, J.D., Dagnelie, G., Katona, S., Greenberg, R., & Suzuki, S. (1999). Pattern electrical stimulation of the human retina. Vision Research 39, 2569–2576.CrossRefGoogle Scholar
Kara, P., Pezaris, J.S., Yurgenson, S., & Reid, R.C. (2002). The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation. Proceedings of the National Academy of Sciences of the U.S.A. 99, 16261–16266.CrossRefGoogle Scholar
Mitzdorf, U. (1985). Current source–density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiological Reviews 65.1, 37–100.Google Scholar
Mitzdorf, U. (1987). Properties of the evoked potential generators: Current source–density analysis of visually evoked potentials in the cat cortex. Journal of Neuroscience 33, 33–59.CrossRefGoogle Scholar
Motokawa, K. & Ebe, M. (1952). Selective stimulation of color receptors with alternating currents. Science 116, 92–94.CrossRefGoogle Scholar
Normann, R.A., Maynard, E.M., Guillory, K., & Warren, D.J. (1996). Cortical implants for the blind. IEEE Spectrum 33, 54–59.CrossRefGoogle Scholar
Normann, R.A., Maynard, E.M., Rousche, P.J., & Warren, D.J. (1999). A neural interface for a cortical vision prosthesis. Vision Research 39, 2577–2587.CrossRefGoogle Scholar
Rager, G. & Singer, W. (1998). The response of cat visual cortex to flicker stimuli of variable frequency. European Journal of Neuroscience 10, 1856–1877.CrossRefGoogle Scholar
Reid, R.C., Victor, J.D., & Shapley, R.M. (1997). The use of m-sequences in the analysis of visual neurons: Linear receptive-field properties. Visual Neuroscience 14, 1015–1027.CrossRefGoogle Scholar
Reitböck, H.J. (1983). Fiber microelectrodes for electrophysiological recordings. Journal of Neuoscience Methods 8, 249–262.CrossRefGoogle Scholar
Santos, A., Humayun, M., de Juan, E., Greenburg, R.J., Marsh, M., Klock, I., & Milam, A. (1997). Preservation of the inner retina in retinitis pigmentosa. Archive Ophthalmology 115, 511–515.CrossRefGoogle Scholar
Schanze, T., Eckhorn, R., Hesse, L., Eger, M., Wilms, M., Kossler, R., & Nebeling, B. (1998). Experimental setup for assessing the efficacy and quality of retina implant stimulations by retinal and cortical recording in cat. Proceedings of the 26th Göttingen Neurobiology Conference, 475.Google Scholar
Schanze, T., Wilms, M., Eger, M., Hesse, L., & Eckhorn, R. (2002). Activation zones in cat visual cortex evoked by electrical retina stimulation. Graefe's Archive of Clinical and Experimental Ophthalmology 240, 947–954.CrossRefGoogle Scholar
Schmidt, E.M., Bak, M.J., Hambrecht, F.T., Kufta, C.V., O'Rourke, D.K., & Vallabhanath, P. (1996). Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. Brain 119, 507–522.CrossRefGoogle Scholar
Seiler, M.J., Aramant, R.B., & Ball, S.L. (1999). Photoreceptor function of retinal transplants implicated by light–dark shift of s-antigen and rod transducin. Vision Research 39, 2589–2596.CrossRefGoogle Scholar
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology (London) 218, 267–283.CrossRefGoogle Scholar
Slovin, H., Arieli, A., Hildesheim, R., & Grinvald, A. (2002). Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. Journal of Neurophysiology 88, 3421–3438.CrossRefGoogle Scholar
Stett, A., Barth, W., Weiss, S., Haemmerle, H., & Zrenner, E. (2000). Electrical multisite stimulation of the isolated chicken retina. Vision Research 40, 1785–1795.CrossRefGoogle Scholar
Sutter, E.E. (1987). A practical nonstochastic approach to nonlinear time-domain analysis. In Advanced Methods of Physiological System Modeling, ed. Marmarelis, V.Z., pp. 303–315. Los Angeles, California: Biomedical Simulations Resource, University of Southern California.
Tusa, R.J., Palmer, L.A., & Rosenquist, A.C. (1979). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.Google Scholar
Veraart, C., Raftopoulos, C., Mortimer, J.T., Delbeke, J., Pins, D., Michaux, G., Vanlierde, A., Parrini, S., & Wanet-Defalque, M.-C. (1998). Visual sensations produced by optic nerve stimulation using an implanted self-sizing spiral cuff electrode. Brain Research 813, 181–186.CrossRefGoogle Scholar
Wilms, M. (2001). Electrical receptive fields and cortical activation spread in response to electrical retina stimulation. Assessment of spatio-temporal resolution for a retina implant. Ph.D. Thesis, Philipps University Marburg.
Wilms, M., Schanze, T., Eger, M., & Eckhorn, R. (2001). Cortical activity distributions in cat area 17/18 elicited by short visual and electrical retinal point stimuli: Investigations for a retina-implant. Proceedings of the 28th Göttingen Neurobiology Conference, 588.Google Scholar
Wyatt, J. & Rizzo, J. (1996). Ocular implants for the blind. IEEE Spectrum 33, 47–53.CrossRefGoogle Scholar
Zrenner, E. (2002). Will retinal implants restore vision? Science 295, 1022–1025.Google Scholar
Zrenner, E., Miliczek, K.D., Gabel, V., Graf, H., Guenther, E., Haemmerle, H., Hoefflinger, B., Kohler, K., Nisch, W., Schubert, M., Stett, A., & Weiss, S. (1997). The development of subretinal microphotodiodes for replacement of degenerated photoreceptors. Ophthalmic Research 29, 269–280.CrossRefGoogle Scholar