An extraocular electrical stimulation approach to slow down the progression of retinal degeneration in an animal model.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
23 09 2023
23 09 2023
Historique:
received:
26
04
2023
accepted:
12
08
2023
medline:
25
9
2023
pubmed:
24
9
2023
entrez:
23
9
2023
Statut:
epublish
Résumé
Retinal diseases such as retinitis pigmentosa (RP) and age-related macular degeneration (AMD) are characterized by unrelenting neuronal death. However, electrical stimulation has been shown to induce neuroprotective changes in the retina capable of slowing down the progression of retinal blindness. In this work, a multi-scale computational model and modeling platform were used to design electrical stimulation strategies to better target the bipolar cells (BCs), that along with photoreceptors are affected at the early stage of retinal degenerative diseases. Our computational findings revealed that biphasic stimulus pulses of long pulse duration could decrease the activation threshold of BCs, and the differential stimulus threshold between ganglion cells (RGCs) and BCs, offering the potential of targeting the BCs during the early phase of degeneration. In vivo experiments were performed to evaluate the electrode placement and parameters found to target bipolar cells and evaluate the safety and efficacy of the treatment. Results indicate that the proposed transcorneal Electrical Stimulation (TES) strategy can attenuate retinal degeneration in a Royal College of Surgeon (RCS) rodent model, offering the potential to translate this work to clinical practice.
Identifiants
pubmed: 37741821
doi: 10.1038/s41598-023-40547-1
pii: 10.1038/s41598-023-40547-1
pmc: PMC10517961
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
15924Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2023. Springer Nature Limited.
Références
Wang, A. L., Knight, D. K., Vu, T. T. & Mehta, M. C. Retinitis Pigmentosa: Review of current treatment. Int. Ophthalmol. Clin. 59(1), 263–280 (2019).
doi: 10.1097/IIO.0000000000000256
pubmed: 30585930
Zhang, Q. Retinitis pigmentosa: Progress and perspective. Asia Pac. J. Ophthalmol. 5, 265–271 (2016).
doi: 10.1097/APO.0000000000000227
Hamel, C. Retinitis pigmentosa. Orphanet J. Rare Dis. 1, 40–52 (2006).
doi: 10.1186/1750-1172-1-40
pubmed: 17032466
pmcid: 1621055
Daiger, S. P., Sullivan, L. S. & Bowne, S. J. Genes and mutations causing retinitis pigmentosa. Clin. Genet. 84, 132–141 (2013).
doi: 10.1111/cge.12203
pubmed: 23701314
Lan, Y. et al. Retina–electrode interface properties and vision restoration by two generations of retinal prostheses in one patient—one in each eye. J. Neural Eng. 17, 026020 (2020).
doi: 10.1088/1741-2552/ab7c8f
Morimoto, T. et al. Transcorneal electrical stimulation promotes the survival of photoreceptors and preserves retinal function in royal college of surgeons rats. Investig. Ophthalmol. Vis. Sci. 48, 4725–4732 (2007).
doi: 10.1167/iovs.06-1404
Morimoto, T. et al. Transcorneal electrical stimulation rescues axotomized retinal ganglion cells by activating endogenous retinal igf-1 system. Investig. Ophthalmol. Vis. Sci. 46, 2147–2155 (2005).
doi: 10.1167/iovs.04-1339
Fu, L. et al. The role of electrical stimulation therapy in ophthalmic diseases. Graefe’s Arch. For Clin. Exp. Ophthalmol. 253, 171–176 (2015).
doi: 10.1007/s00417-014-2889-7
Sehic, A. et al. Electrical stimulation as a means for improving vision. Am. J. Pathol. 186, 2783–2797 (2016).
doi: 10.1016/j.ajpath.2016.07.017
pubmed: 27643530
pmcid: 5225285
Cela, C. J. A multiresolution admittance method for large-scale bioelectromagnetic interactions. Ph.D. thesis, North Carolina State University (2010).
Paknahad, J., Humayun, M. & Lazzi, G. Selective activation of retinal ganglion cell subtypes through targeted electrical stimulation parameters. IEEE Trans. Neural Syst. Rehabil. Eng. 30, 350–359 (2022).
doi: 10.1109/TNSRE.2022.3149967
pubmed: 35130164
pmcid: 8904155
Paknahad, J., Kosta, P., Bouteiller, J. M. C., Humayun, M. S. & Lazzi, G. Mechanisms underlying activation of retinal bipolar cells through targeted electrical stimulation: a computational study. J. Neural Eng. 18(6), 066034 (2021).
doi: 10.1088/1741-2552/ac3dd8
Paknahad, J., Kosta, P., Iseri, E., Farzad, S., Bouteiller, J. M. C., Humayun, M. S., & Lazzi, G. Modeling ON cone bipolar cells for electrical stimulation. In 2021 43rd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC) 6547–6550. (IEEE, 2021).
Paknahad, J., Kosta, P., Bouteiller, J. M. C., Humayun, M. S. & Lazzi, G. The sensitivity of retinal bipolar cells response to long stimulus pulse durations in epiretinal prostheses. Investig. Ophthalmol. Vis. Sci. 62(8), 3169–3169 (2021).
Paknahad, J., Loizos, K., Yue, L., Humayun, M. S. & Lazzi, G. Color and cellular selectivity of retinal ganglion cell subtypes through frequency modulation of electrical stimulation. Sci. Rep. 11(1), 5177 (2021).
doi: 10.1038/s41598-021-84437-w
pubmed: 33664347
pmcid: 7933163
Iseri, E., Kosta, P., Paknahad, J., Bouteiller, J. M. C., & Lazzi, G. A computational model simulates light-evoked responses in the retinal cone pathway. In 2021 43rd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), 4482–4486 (IEEE, 2021).
Kosta, P. et al. Model-based comparison of current flow in rod bipolar cells of healthy and early-stage degenerated retina. Exp. Eye Res. 207, 108554 (2021).
doi: 10.1016/j.exer.2021.108554
pubmed: 33794197
pmcid: 8187309
Paknahad, J., Loizos, K., Humayun, M. & Lazzi, G. Targeted stimulation of retinal ganglion cells in epiretinal prostheses: A multiscale computational study. IEEE Trans. Neural Syst. Rehabil. Eng. 28(11), 2548–2556 (2020).
doi: 10.1109/TNSRE.2020.3027560
pubmed: 32991284
pmcid: 7737501
Paknahad, J., Loizos, K., Humayun, M., & Lazzi, G. Responsiveness of retinal ganglion cells through frequency modulation of electrical stimulation: A computational modeling study. In 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), 3393–3398 (IEEE, 2020).
Kosta, P., Loizos, K. & Lazzi, G. Stimulus waveform design for decreasing charge and increasing stimulation selectivity in retinal prostheses. Healthc. Technol. Lett. 7(3), 66–71 (2020).
doi: 10.1049/htl.2019.0115
pubmed: 32754340
pmcid: 7353818
Mendes, B. M., de Almeida, I. G., Trindade, B. M., Fonseca, T. C. F. & de Campos, T. P. R. Development of a mouse computational model for MCNPx based on Digimouse(r) images and dosimetric assays. Braz. J. Pharm. Sci. 53, e16092 (2017).
doi: 10.1590/s2175-97902017000116092
Italian National Research Council - Institute for Applied Physics (CNR-IFAC). An Internet resource for the calculation of the Dielectric Properties of Body Tissues in the frequency range 10 Hz–100 GHz. http://niremf.ifac.cnr.it/tissprop/.
Carnevale, N. T. & Hines, M. L. The NEURON Book (Cambridge University Press, 2006).
doi: 10.1017/CBO9780511541612
Rattay, F., Bassereh, H. & Stiennon, I. Compartment models for the electrical stimulation of retinal bipolar cells. PLoS ONE 13(12), e0209123 (2018).
doi: 10.1371/journal.pone.0209123
pubmed: 30557410
pmcid: 6296559
Werginz, P. & Rattay, F. The impact of calcium current reversal on neurotransmitter release in the electrically stimulated retina. JNE. 13(4), 046013 (2016).
pubmed: 27296730
Qin, W. et al. Single-compartment models of retinal ganglion cells with different electrophysiologies. Network 28, 74–93 (2017).
doi: 10.1080/0954898X.2018.1455993
pubmed: 29649919
Ascoli, G. A. Mobilizing the base of neuroscience data: The case of neuronal morphologies. Nat. Rev. Neurosci. 7, 318–324 (2006).
doi: 10.1038/nrn1885
pubmed: 16552417
Strauss, O., Stumpff, F., Mergler, S., Wienrich, M. & Wiederholt, M. The Royal College of Surgeons rat: an animal model for inherited retinal degeneration with a still unknown genetic defect. Acta Anat. 162(2–3), 101–111. https://doi.org/10.1159/000046474 (1998).
doi: 10.1159/000046474
pubmed: 9831756
Thomas, B. B., Seiler, M. J., Sadda, S. R. & Aramant, R. B. Superior colliculus responses to light-preserved by transplantation in a slow degeneration rat model. Exp. Eye Res. 79(1), 29–39 (2004).
doi: 10.1016/j.exer.2004.02.016
pubmed: 15183098
Bubis, E. et al. Blue autofluorescence fundus imaging for monitoring retinal degeneration in royal college of surgeons rats. Transl Vis Sci Technol. 8(1), 26. https://doi.org/10.1167/tvst.8.1.26 (2019).
doi: 10.1167/tvst.8.1.26
pubmed: 30834174
pmcid: 6396687
Rattay, F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 89(2), 335–346. https://doi.org/10.1016/S0306-4522(98)00330-3 (1999).
doi: 10.1016/S0306-4522(98)00330-3
pubmed: 10077317
Rattay, F. Analysis of models for external stimulation of axons. In IEEE Transactions on Biomedical Engineering, vol. BME-33, no. 10, 974–977 https://doi.org/10.1109/TBME.1986.325670 (1986).
Werginz, P., Wang, B. Y., Chen, Z. C. & Palanker, D. On optimal coupling of the “electronic photoreceptors” into the degenerate retina. J. Neural Eng. 17(4), 045008 (2020).
doi: 10.1088/1741-2552/aba0d2
pubmed: 32613948
Walston, S. T., Chow, R. H. & Weiland, J. D. Direct measurement of bipolar cell responses to electrical stimulation in wholemount mouse retina. J. Neural Eng. 15, 046003 (2018).
doi: 10.1088/1741-2552/aab4ed
pubmed: 29513646
pmcid: 6657336
Shannon, R. V. A model of safe levels for electrical stimulation. IEEE Trans. Biomed. Eng. 39(4), 424–426. https://doi.org/10.1109/10.126616 (1992).
doi: 10.1109/10.126616
pubmed: 1592409
Miyake, K.-I., Yoshida, M., Inoue, Y. & Hata, Y. Neuroprotective effect of transcorneal electrical stimulation on the acute phase of optic nerve injury. Investig. Ophthalmol. Vis. Sci. 48, 2356–2361 (2007).
doi: 10.1167/iovs.06-1329
Yu, H. et al. Noninvasive electrical stimulation improves photoreceptor survival and retinal function in mice with inherited photoreceptor degeneration. Investig. Ophthalmol. Vis. Sci. 61, 5–5 (2020).
doi: 10.1167/iovs.61.4.5
Henrich-Noack, P., Sergeeva, E. G. & Sabel, B. A. Non-invasive electrical brain stimulation: From acute to late-stage treatment of central nervous system damage. Neural Regen. Res. 12, 1590 (2017).
doi: 10.4103/1673-5374.217322
pubmed: 29171414
pmcid: 5696830
Xie, J. et al. Modeling and percept of transcorneal electrical stimulation in humans. IEEE Trans. Biomed. Eng. 58, 1932–1939 (2010).
doi: 10.1109/TBME.2010.2087378
pubmed: 20952323
Potts, A. M., Inoue, J. & Buffum, D. The electrically evoked response of the visual system (eer). Investig. Ophthalmol. 7, 269–278 (1968).
Pan, Z. H. & Hu, H. J. Voltage-dependent Na(+) currents in mammalian retinal cone bipolar cells. J. Neurophysiol. 84(5), 2564–2571 (2000).
doi: 10.1152/jn.2000.84.5.2564
pubmed: 11067998
Cui, J. & Pan, Z. Two types of cone bipolar cells express voltage-gated Na channels in the rat retina. Vis. Neurosci. 25(5–6), 635–645. https://doi.org/10.1017/S0952523808080851 (2008).
doi: 10.1017/S0952523808080851
pubmed: 19094370
pmcid: 2650833
Willmann, G. et al. Gene expression profiling of the retina after transcorneal electrical stimulation in wild-type Brown Norway rats. Investig. Ophthalmol. Vis. Sci. 52, 7529–7537 (2011).
doi: 10.1167/iovs.11-7838