Neural responses to multielectrode stimulation of healthy and degenerate retina

Kerry J. Halupka, Carla J. Abbott, Yan T. Wong, Shaun L. Cloherty, David B Grayden, Anthony N. Burkitt, Evgeni N. Sergeev, Chi D Luu, Alice Brandli, Penelope Jayne Allen, Hamish Meffin, Mohit N. Shivdasani

Research output: Contribution to journalArticleResearchpeer-review

9 Citations (Scopus)

Abstract

PURPOSE. Simultaneous stimulation of multiple retinal electrodes in normally sighted animals shows promise in improving the resolution of retinal prostheses. However, the effects of simultaneous stimulation on degenerate retinae remain unknown. Therefore, we investigated the characteristics of cortical responses to multielectrode stimulation of the degenerate retina. METHODS. Four adult cats were bilaterally implanted with retinal electrode arrays in the suprachoroidal space after unilateral adenosine triphosphate (ATP)–induced retinal photoreceptor degeneration. Functional and structural changes were characterized by using electroretinogram a-wave amplitude and optical coherence tomography. Multiunit activity was recorded from both hemispheres of the visual cortex. Responses to single- and multielectrode stimulation of the ATP-injected and fellow control eyes were characterized and compared. RESULTS. The retinae of ATP-injected eyes displayed structural and functional changes consistent with mid- to late-stage photoreceptor degeneration and remodeling. Responses to multielectrode stimulation of the ATP-injected eyes exhibited shortened latencies, lower saturated spike counts, and higher thresholds, compared to stimulation of the fellow control eyes. Electrical receptive field sizes were significantly larger in the ATP-injected eye than in the control eye, and positively correlated with the extent of degeneration. CONCLUSIONS. Significant differences exist between cortical responses to stimulation of healthy and degenerate retinae. Our results highlight the importance of using a retinal degeneration model when evaluating the efficacy of novel stimulation paradigms.

Original languageEnglish
Pages (from-to)3770-3784
Number of pages15
JournalInvestigative Ophthalmology and Visual Science
Volume58
Issue number9
DOIs
Publication statusPublished - 1 Jul 2017

Keywords

  • Computational modeling
  • Electrical stimulation
  • In vivo electrophysiology
  • Retinal degeneration
  • Retinal prosthesis

Cite this

Halupka, K. J., Abbott, C. J., Wong, Y. T., Cloherty, S. L., Grayden, D. B., Burkitt, A. N., ... Shivdasani, M. N. (2017). Neural responses to multielectrode stimulation of healthy and degenerate retina. Investigative Ophthalmology and Visual Science, 58(9), 3770-3784. https://doi.org/10.1167/iovs.16-21290
Halupka, Kerry J. ; Abbott, Carla J. ; Wong, Yan T. ; Cloherty, Shaun L. ; Grayden, David B ; Burkitt, Anthony N. ; Sergeev, Evgeni N. ; Luu, Chi D ; Brandli, Alice ; Allen, Penelope Jayne ; Meffin, Hamish ; Shivdasani, Mohit N. / Neural responses to multielectrode stimulation of healthy and degenerate retina. In: Investigative Ophthalmology and Visual Science. 2017 ; Vol. 58, No. 9. pp. 3770-3784.
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title = "Neural responses to multielectrode stimulation of healthy and degenerate retina",
abstract = "PURPOSE. Simultaneous stimulation of multiple retinal electrodes in normally sighted animals shows promise in improving the resolution of retinal prostheses. However, the effects of simultaneous stimulation on degenerate retinae remain unknown. Therefore, we investigated the characteristics of cortical responses to multielectrode stimulation of the degenerate retina. METHODS. Four adult cats were bilaterally implanted with retinal electrode arrays in the suprachoroidal space after unilateral adenosine triphosphate (ATP)–induced retinal photoreceptor degeneration. Functional and structural changes were characterized by using electroretinogram a-wave amplitude and optical coherence tomography. Multiunit activity was recorded from both hemispheres of the visual cortex. Responses to single- and multielectrode stimulation of the ATP-injected and fellow control eyes were characterized and compared. RESULTS. The retinae of ATP-injected eyes displayed structural and functional changes consistent with mid- to late-stage photoreceptor degeneration and remodeling. Responses to multielectrode stimulation of the ATP-injected eyes exhibited shortened latencies, lower saturated spike counts, and higher thresholds, compared to stimulation of the fellow control eyes. Electrical receptive field sizes were significantly larger in the ATP-injected eye than in the control eye, and positively correlated with the extent of degeneration. CONCLUSIONS. Significant differences exist between cortical responses to stimulation of healthy and degenerate retinae. Our results highlight the importance of using a retinal degeneration model when evaluating the efficacy of novel stimulation paradigms.",
keywords = "Computational modeling, Electrical stimulation, In vivo electrophysiology, Retinal degeneration, Retinal prosthesis",
author = "Halupka, {Kerry J.} and Abbott, {Carla J.} and Wong, {Yan T.} and Cloherty, {Shaun L.} and Grayden, {David B} and Burkitt, {Anthony N.} and Sergeev, {Evgeni N.} and Luu, {Chi D} and Alice Brandli and Allen, {Penelope Jayne} and Hamish Meffin and Shivdasani, {Mohit N.}",
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Halupka, KJ, Abbott, CJ, Wong, YT, Cloherty, SL, Grayden, DB, Burkitt, AN, Sergeev, EN, Luu, CD, Brandli, A, Allen, PJ, Meffin, H & Shivdasani, MN 2017, 'Neural responses to multielectrode stimulation of healthy and degenerate retina', Investigative Ophthalmology and Visual Science, vol. 58, no. 9, pp. 3770-3784. https://doi.org/10.1167/iovs.16-21290

Neural responses to multielectrode stimulation of healthy and degenerate retina. / Halupka, Kerry J.; Abbott, Carla J.; Wong, Yan T.; Cloherty, Shaun L.; Grayden, David B; Burkitt, Anthony N.; Sergeev, Evgeni N.; Luu, Chi D; Brandli, Alice; Allen, Penelope Jayne; Meffin, Hamish; Shivdasani, Mohit N.

In: Investigative Ophthalmology and Visual Science, Vol. 58, No. 9, 01.07.2017, p. 3770-3784.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Neural responses to multielectrode stimulation of healthy and degenerate retina

AU - Halupka, Kerry J.

AU - Abbott, Carla J.

AU - Wong, Yan T.

AU - Cloherty, Shaun L.

AU - Grayden, David B

AU - Burkitt, Anthony N.

AU - Sergeev, Evgeni N.

AU - Luu, Chi D

AU - Brandli, Alice

AU - Allen, Penelope Jayne

AU - Meffin, Hamish

AU - Shivdasani, Mohit N.

PY - 2017/7/1

Y1 - 2017/7/1

N2 - PURPOSE. Simultaneous stimulation of multiple retinal electrodes in normally sighted animals shows promise in improving the resolution of retinal prostheses. However, the effects of simultaneous stimulation on degenerate retinae remain unknown. Therefore, we investigated the characteristics of cortical responses to multielectrode stimulation of the degenerate retina. METHODS. Four adult cats were bilaterally implanted with retinal electrode arrays in the suprachoroidal space after unilateral adenosine triphosphate (ATP)–induced retinal photoreceptor degeneration. Functional and structural changes were characterized by using electroretinogram a-wave amplitude and optical coherence tomography. Multiunit activity was recorded from both hemispheres of the visual cortex. Responses to single- and multielectrode stimulation of the ATP-injected and fellow control eyes were characterized and compared. RESULTS. The retinae of ATP-injected eyes displayed structural and functional changes consistent with mid- to late-stage photoreceptor degeneration and remodeling. Responses to multielectrode stimulation of the ATP-injected eyes exhibited shortened latencies, lower saturated spike counts, and higher thresholds, compared to stimulation of the fellow control eyes. Electrical receptive field sizes were significantly larger in the ATP-injected eye than in the control eye, and positively correlated with the extent of degeneration. CONCLUSIONS. Significant differences exist between cortical responses to stimulation of healthy and degenerate retinae. Our results highlight the importance of using a retinal degeneration model when evaluating the efficacy of novel stimulation paradigms.

AB - PURPOSE. Simultaneous stimulation of multiple retinal electrodes in normally sighted animals shows promise in improving the resolution of retinal prostheses. However, the effects of simultaneous stimulation on degenerate retinae remain unknown. Therefore, we investigated the characteristics of cortical responses to multielectrode stimulation of the degenerate retina. METHODS. Four adult cats were bilaterally implanted with retinal electrode arrays in the suprachoroidal space after unilateral adenosine triphosphate (ATP)–induced retinal photoreceptor degeneration. Functional and structural changes were characterized by using electroretinogram a-wave amplitude and optical coherence tomography. Multiunit activity was recorded from both hemispheres of the visual cortex. Responses to single- and multielectrode stimulation of the ATP-injected and fellow control eyes were characterized and compared. RESULTS. The retinae of ATP-injected eyes displayed structural and functional changes consistent with mid- to late-stage photoreceptor degeneration and remodeling. Responses to multielectrode stimulation of the ATP-injected eyes exhibited shortened latencies, lower saturated spike counts, and higher thresholds, compared to stimulation of the fellow control eyes. Electrical receptive field sizes were significantly larger in the ATP-injected eye than in the control eye, and positively correlated with the extent of degeneration. CONCLUSIONS. Significant differences exist between cortical responses to stimulation of healthy and degenerate retinae. Our results highlight the importance of using a retinal degeneration model when evaluating the efficacy of novel stimulation paradigms.

KW - Computational modeling

KW - Electrical stimulation

KW - In vivo electrophysiology

KW - Retinal degeneration

KW - Retinal prosthesis

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DO - 10.1167/iovs.16-21290

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SN - 1552-5783

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