Spatially selective activation of the visual cortex via intraneural stimulation of the optic nerve.
Journal
Nature biomedical engineering
ISSN: 2157-846X
Titre abrégé: Nat Biomed Eng
Pays: England
ID NLM: 101696896
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
25
04
2018
accepted:
18
07
2019
pubmed:
21
8
2019
medline:
6
5
2020
entrez:
21
8
2019
Statut:
ppublish
Résumé
Retinal prostheses can restore a functional form of vision in patients affected by dystrophies of the outer retinal layer. Beyond clinical utility, prostheses for the stimulation of the optic nerve, the visual thalamus or the visual cortex could also serve as tools for studying the visual system. Optic-nerve stimulation is particularly promising because it directly activates nerve fibres, takes advantage of the high-level information processing occurring downstream in the visual pathway, does not require optical transparency and could be effective in cases of eye trauma. Here we show, in anaesthetized rabbits and with support from numerical modelling, that an intraneural electrode array with high mechanical stability placed in the intracranial segment of the optic nerve induces, on electrical stimulation, selective activation patterns in the visual cortex. These patterns are measured as electrically evoked cortical potentials via an ECoG array placed in the contralateral cortex. The intraneural electrode array should enable further investigations of the effects of electrical stimulation in the visual system and could be further developed as a visual prosthesis for blind patients.
Identifiants
pubmed: 31427779
doi: 10.1038/s41551-019-0446-8
pii: 10.1038/s41551-019-0446-8
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
181-194Commentaires et corrections
Type : CommentIn
Références
Bourne, R. R. et al. Causes of vision loss worldwide, 1990–2010: a systematic analysis. Lancet Glob. Health 1, e339–e349 (2013).
pubmed: 25104599
Brindley, G. & Lewin, W. The sensations produced by electrical stimulation of the visual cortex. J. Physiol. 196, 479–493 (1968).
pubmed: 4871047
pmcid: 1351724
Dobelle, W., Mladejovsky, M. & Girvin, J. Artificial vision for the blind: Electrical stimulation of visual cortex offers hope for a functional prosthesis. Science 183, 440–444 (1974).
pubmed: 4808973
Zrenner, E. Fighting blindness with microelectronics. Sci. Transl. Med. 5, 210ps16 (2013).
pubmed: 24197733
Ghezzi, D. Retinal prostheses: progress toward the next generation implants. Front. Neurosci. 9, 290 (2015).
pubmed: 26347602
pmcid: 4542462
Stingl, K. et al. Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS. Proc. R. Soc. B 280, 20130077 (2013).
pubmed: 23427175
da Cruz, L. et al. Five-year safety and performance results from the Argus II retinal prosthesis system clinical trial. Ophthalmology 123, 2248–2254 (2016).
pubmed: 27453256
pmcid: 5035591
Ayton, L. N. et al. First-in-human trial of a novel suprachoroidal retinal prosthesis. PLoS ONE 9, e115239 (2014).
Brelén, M. E., Vince, V., Gérard, B., Veraart, C. & Delbeke, J. Measurement of evoked potentials after electrical stimulation of the human optic nerve. Invest. Ophthalmol. Vis. Sci. 51, 5351–5355 (2010).
pubmed: 20463320
Panetsos, F., Sanchez-Jimenez, A., Cerio, E., Diaz-Guemes, I. & Sanchez, F. M. Consistent phosphenes generated by electrical microstimulation of the visual thalamus. An experimental approach for thalamic visual neuroprostheses. Front. Neurosci. 5, 84 (2011).
pubmed: 21779233
pmcid: 3132634
Normann, R. A. et al. Toward the development of a cortically based visual neuroprosthesis. J. Neural Eng. 6, 035001 (2009).
pubmed: 19458403
pmcid: 2941645
Merabet, L. B., Rizzo, J. F., Amedi, A., Somers, D. C. & Pascual-Leone, A. What blindness can tell us about seeing again: merging neuroplasticity and neuroprostheses. Nat. Rev. Neurosci. 6, 71–77 (2005).
pubmed: 15611728
Luo, Y. & da Cruz, L. The Argus II retinal prosthesis system. Prog. Retin. Eye Res. 50, 89–107 (2016).
pubmed: 26404104
Stingl, K. et al. Subretinal visual implant Alpha IMS—Clinical trial interim report. Vis. Res. 111, 149–160 (2015).
pubmed: 25812924
Lorach, H. et al. Photovoltaic restoration of sight with high visual acuity. Nat. Med. 21, 476–482 (2015).
pubmed: 4601644
pmcid: 4601644
Ferlauto, L. et al. Design and validation of a foldable and photovoltaic wide-field epiretinal prosthesis. Nat. Commun. 9, 992 (2018).
pubmed: 29520006
pmcid: 5843635
Antognazza, M. et al. Shedding light on living cells. Adv. Mater. 27, 7662–7669 (2015).
pubmed: 25469452
Maya-Vetencourt, J. et al. A fully organic retinal prosthesis restores vision in a rat model of degenerative blindness. Nat. Mater. 16, 681–689 (2017).
pubmed: 28250420
pmcid: 5446789
Antognazza, M. et al. Characterization of a polymer‐based, fully organic prosthesis for implantation into the subretinal space of the rat. Adv. Health. Mater. 5, 2271–2282 (2016).
Veraart, C. et al. Visual sensations produced by optic nerve stimulation using an implanted self-sizing spiral cuff electrode. Brain Res. 813, 181–186 (1998).
pubmed: 9824694
Brelén, M. E. et al. Intraorbital implantation of a stimulating electrode for an optic nerve visual prosthesis. J. Neurosur. 104, 593–597 (2006).
Duret, F. et al. Object localization, discrimination, and grasping with the optic nerve visual prosthesis. Restor. Neurol. Neurosci. 24, 31–40 (2006).
pubmed: 16518026
Veraart, C., Wanet‐Defalque, M., Gérard, B., Vanlierde, A. & Delbeke, J. Pattern recognition with the optic nerve visual prosthesis. Artif. Organs 27, 996–1004 (2003).
pubmed: 14616518
Brelén, M., Duret, F., Gérard, B., Delbeke, J. & Veraart, C. Creating a meaningful visual perception in blind volunteers by optic nerve stimulation. J. Neural Eng. 2, S22 (2005).
pubmed: 15876651
The Lasker/IRRF Initiative for Innovation in Vision Science. Chapter 1 - Restoring vision to the blind: The new age of implanted visual prostheses. Transl. Vis. Sci. Technol. https://doi.org/10.1167/tvst.3.7.3 (2014).
Yan, Y. et al. Electrically evoked responses in the rabbit cortex induced by current steering with penetrating optic nerve electrodes. Invest. Ophthalmol. Vis. Sci. 57, 6327–6338 (2016).
pubmed: 27893099
Sun, J., Chen, Y., Chai, X., Ren, Q. & Li, L. Penetrating electrode stimulation of the rabbit optic nerve: parameters and effects on evoked cortical potentials. Graefes Arch. Clin. Exp. Ophthalmol. 251, 2545–2554 (2013).
pubmed: 24013577
Lu, Y. et al. Electrical stimulation with a penetrating optic nerve electrode array elicits visuotopic cortical responses in cats. J. Neural Eng. 10, 036022 (2013).
pubmed: 23665847
Raspopovic, S. et al. Restoring natural sensory feedback in real-time bidirectional hand prostheses. Sci. Transl. Med. 6, 222ra19–222ra19 (2014).
pubmed: 24500407
Oddo, C. et al. Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans. eLife 5, e09148 (2016).
pubmed: 26952132
pmcid: 4798967
Raspopovic, S., Capogrosso, M., Badia, J., Navarro, X. & Micera, S. Experimental validation of a hybrid computational model for selective stimulation using transverse intrafascicular multichannel electrodes. IEEE Trans. Neural Syst. Rehabil. Eng. 20, 395–404 (2012).
pubmed: 22481834
Badia, J. et al. Comparative analysis of transverse intrafascicular multichannel, longitudinal intrafascicular and multipolar cuff electrodes for the selective stimulation of nerve fascicles. J. Neural Eng. 8, 036023 (2011).
pubmed: 21558601
Cutrone, A. et al. A three-dimensional self-opening intraneural peripheral interface (SELINE). J. Neural Eng. 12, 016016 (2015).
pubmed: 25605565
Wurth, S. et al. Long-term usability and bio-integration of polyimide-based intra-neural stimulating electrodes. Biomaterials 122, 114–129 (2017).
pubmed: 28110171
Hukins, D. W. L., Mahomed, A. & Kukureka, S. N. Accelerated aging for testing polymeric biomaterials and medical devices. Med. Eng. Phys. 30, 1270–1274 (2008).
pubmed: 18692425
Howlader, M., Doyle, T., Mohtashami, S. & Kish, J. Charge transfer and stability of implantable electrodes on flexible substrate. Sens. Actuators B Chem. 178, 132–139 (2013).
Giolli, R. & Guthrie The primary optic projections in the rabbit. An experimental degeneration study. J. Com. Neurol. 136, 99–126 (1969).
Sun, J. et al. Spatiotemporal properties of multipeaked electrically evoked potentials elicited by penetrative optic nerve stimulation in rabbits. Invest. Ophthalmol. Vis. Sci. 52, 146–154 (2011).
pubmed: 20720225
Delorme, A., Palmer, J., Onton, J., Oostenveld, R. & Makeig, S. Independent EEG sources are dipolar. PLoS ONE 7, e30135 (2012).
pubmed: 22355308
pmcid: 3280242
Menicucci, D. et al. Brain responses to emotional stimuli during breath holding and hypoxia: an approach based on the independent component analysis. Brain Topogr. 27, 771–785 (2014).
pubmed: 24375284
Artoni, F. et al. Unidirectional brain to muscle connectivity reveals motor cortex control of leg muscles during stereotyped walking. NeuroImage 159, 403–416 (2017).
pubmed: 28782683
pmcid: 6698582
Bell, A. & Sejnowski, T. An information-maximization approach to blind separation and blind deconvolution. Neural Comput. 7, 1129–1159 (1995).
Delbeke, J., Oozeer, M. & Veraart, C. Position, size and luminosity of phosphenes generated by direct optic nerve stimulation. Vis. Res. 43, 1091–1102 (2003).
pubmed: 12676250
Li, M. et al. A simulation of current focusing and steering with penetrating optic nerve electrodes. J. Neural Eng. 10, 066007 (2013).
pubmed: 24140618
Ghezzi, D. et al. A polymer optoelectronic interface restores light sensitivity in blind rat retinas. Nat. Photonics 7, 400–406 (2013).
pubmed: 27158258
pmcid: 4855023
Mathieson, K. et al. Photovoltaic retinal prosthesis with high pixel density. Nat. Photonics 6, 391–397 (2012).
pubmed: 23049619
pmcid: 23049619
Mandel, Y. et al. Cortical responses elicited by photovoltaic subretinal prostheses exhibit similarities to visually evoked potentials. Nat. Commun. 4, 1980 (2013).
pubmed: 23778557
pmcid: 4249937
Tang, J. et al. Nanowire arrays restore vision in blind mice. Nat. Commun. 9, 786 (2018).
pubmed: 29511183
pmcid: 5840349
Sakaguchi, H. et al. Artificial vision by direct optic nerve electrode (AV-DONE) implantation in a blind patient with retinitis pigmentosa. J. Artif. Organs 12, 206–209 (2009).
pubmed: 19894096
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. 11, 026008 (2014).
pubmed: 4082997
pmcid: 4082997
Weiland, J. D., Walston, S. T. & Humayun, M. S. Electrical stimulation of the retina to produce artificial vision. Annu. Rev. Vis. Sci. 2, 273–294 (2016).
pubmed: 28532361
Nirenberg, S. & Pandarinath, C. Retinal prosthetic strategy with the capacity to restore normal vision. Proc. Natl Acad. Sci. USA 109, 15012–15017 (2012).
pubmed: 22891310
Piedade, M., Gerald, J., Sousa, L., Tavares, G. & Tomás, P. Visual neuroprosthesis: a non invasive system for stimulating the cortex. IEEE Trans. Circuits Syst. I 52, 2648–2662 (2005).
Sieu, L.-A. A. et al. EEG and functional ultrasound imaging in mobile rats. Nat. Methods 12, 831–834 (2015).
pubmed: 26237228
pmcid: 4671306
Demene, C. et al. Functional ultrasound imaging of brain activity in human newborns. Sci. Transl. Med. 9, eaah6756 (2017).
pubmed: 29021168
Blaize, K. et al. Functional ultrasound imaging of deep visual cortex in awake non-human primates. Preprint at Biorxiv https://doi.org/10.1101/551663 (2019).
Palmer, J. A., Kreutz-Delgado, K., Rao, B. D. & Makeig, S. in Independent Component Analysis and Signal Separation (eds Davies M.E. et al.) 90–97 (Springer, 2007).
Artoni, F., Menicucci, D., Delorme, A., Makeig, S. & Micera, S. RELICA: a method for estimating the reliability of independent components. NeuroImage 103, 391–400 (2014).
pubmed: 25234117
pmcid: 6656895
Artoni, F., Delorme, A. & Makeig, S. Applying dimension reduction to EEG data by principal component analysis reduces the quality of its subsequent independent component decomposition. NeuroImage 175, 176–187 (2018).
pubmed: 29526744
pmcid: 6650744
Goodall, E. V., Kosterman, L. M., Holsheimer, J. & Struijk, J. J. Modeling study of activation and propagation delays during stimulation of peripheral nerve fibers with a tripolar cuff electrode. IEEE Trans. Rehabil. Eng. 3, 272–282 (1995).
Chintalacharuvu, R. R., Ksienski, D. A. & Mortimer, J. T. A numerical analysis of the electric field generated by a nerve cuff electrode. Proc. Annual International Conference of the IEEE Engineering in Medicine and Biology Society 912-913 (IEEE, 1991).
Struijk, J. J., Holsheimer, J., Barolat, G., He, J. & Boom, H. B. K. Paresthesia thresholds in spinal cord stimulation: a comparison of theoretical results with clinical data. IEEE Trans. Rehabil. Eng. 1, 101–108 (1993).
Bossetti, C. A., Birdno, M. J. & Grill, W. M. Analysis of the quasi-static approximation for calculating potentials generated by neural stimulation. J. Neural Eng. 5, 44 (2008).
pubmed: 18310810
McIntyre, C. C. & Grill, W. M. Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J. Neurophysiol. 88, 1592–1604 (2002).
pubmed: 12364490
Raspopovic, S., Capogrosso, M. & Micera, S. A computational model for the stimulation of rat sciatic nerve using a transverse intrafascicular multichannel electrode. IEEE Trans. Neural Syst. Rehabil. Eng. 19, 333–344 (2011).
pubmed: 21693427
Hodgkin, A. & Huxley, A. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544 (1952).
pubmed: 1392413
pmcid: 1392413
Oozeer, M., Veraart, C., Legat, V. & Delbeke, J. A model of the mammalian optic nerve fibre based on experimental data. Vis. Res. 46, 2513–2524 (2006).
pubmed: 16542698