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Neurotherapeutics

, Volume 16, Issue 1, pp 134–143 | Cite as

Brain Machine Interfaces for Vision Restoration: The Current State of Cortical Visual Prosthetics

  • Soroush Niketeghad
  • Nader PouratianEmail author
Review

Abstract

Loss of vision alters the day to day life of blind individuals and may impose a significant burden on their family and the economy. Cortical visual prosthetics have been shown to have the potential of restoring a useful degree of vision via stimulation of primary visual cortex. Due to current advances in electrode design and wireless power and data transmission, development of these prosthetics has gained momentum in the past few years and multiple sites around the world are currently developing and testing their designs. In this review, we briefly outline the visual prosthetic approaches and describe the history of cortical visual prosthetics. Next, we focus on the state of the art of cortical visual prosthesis by briefly explaining the design of current devices that are either under development or in the clinical testing phase. Lastly, we shed light on the challenges of each design and provide some potential solutions.

Keywords

Blindness Visual prosthetic Stimulation Visual cortex Electrode array Brain computer interface 

Notes

Acknowledgments

The authors would like to thank the SecondSight Inc. for providing a platform that allowed us to have hands on experience with their state of the art cortical visual prosthesis (Orion) and understand some of the challenges of design, implantation, and testing of these devices.

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Disclosure forms provided by the authors are available with the online version of this article.

Supplementary material

13311_2018_660_MOESM1_ESM.pdf (511 kb)
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References

  1. 1.
    Stevens GA, White RA, Flaxman SR, Price H, Jonas JB, Keeffe J, et al. Global prevalence of vision impairment and blindness: Magnitude and temporal trends, 1990-2010. Ophthalmology. 2013;120(12):2377–84.CrossRefGoogle Scholar
  2. 2.
    Varma R, Vajaranant TS, Burkemper B, Wu S, Torres M, Hsu C, et al. Visual impairment and blindness in adults in the United States. JAMA Ophthalmol. 2016;134(7):802–9.CrossRefGoogle Scholar
  3. 3.
    Crews JE, Campbell VA. Vision Impairment and Hearing Loss among Community-Dwelling Older Americans: Implications for Health and Functioning. Am J Public Health. 2004;94(5):823–9.CrossRefGoogle Scholar
  4. 4.
    Ivers RQ, Norton R, Cumming RG, Butler M, Campbell a J. Visual impairment and risk of hip fracture. Am J Epidemiol. 2000;152(7):633–9.CrossRefGoogle Scholar
  5. 5.
    Jones GC, Rovner BW, Crews JE, Danielson ML. Effects of Depressive Symptoms on Health Behavior Practices Among Older Adults With Vision Loss. Rehabil Psychol. 2009;54(2):164–72.CrossRefGoogle Scholar
  6. 6.
    Zhang X, Bullard KMK, Cotch MF, Wilson MR, Rovner BW, McGwin G, et al. Association between depression and functional vision loss in persons 20 years of age or older in the United States, NHANES 2005-2008. JAMA Ophthalmol. 2013;131(5):573–81.CrossRefGoogle Scholar
  7. 7.
    Zheng DD, Christ SL, Lam BL, Tannenbaum SL, Bokman CL, Arheart KL, et al. Visual acuity and increased mortality: The role of allostatic load and functional status. Investig Ophthalmol Vis Sci. 2014;55(8):5144–50.CrossRefGoogle Scholar
  8. 8.
    Freeman EE, Egleston BL, West SK, Bandeen-Roche K, Rubin G. Visual acuity change and mortality in older adults. Invest Ophthalmol Vis Sci. 2005;46:4040–5.CrossRefGoogle Scholar
  9. 9.
    Frick KD, Gower EW, Kempen JH, Wolff JL. Economic impact of visual impairment and blinfdness in the United States. Arch Ophthalmol. 2007;125(4):544–50.CrossRefGoogle Scholar
  10. 10.
    Congdon NG, Friedman DS, Lietman T. Important Causes of Visual Impairment in the World Today. Vol. 290, Journal of the American Medical Association. 2003. p. 2057–60.Google Scholar
  11. 11.
    Oliver JE, Hattenhauer MG, Herman D, Hodge DO, Kennedy R, Fang-Yen M, et al. Blindness and glaucoma: a comparison of patients progressing to blindness from glaucoma with patients maintaining vision. Am J Ophthalmol. 2002;133(6):764–72.CrossRefGoogle Scholar
  12. 12.
    West S, Sommer A. Prevention of blindness and priorities for the future. Bull World Health Organ. 2001;79(3):244–8.Google Scholar
  13. 13.
    Resnikoff S, Pararajasegaram R. Blindness prevention programmes: past, present, and future. Bull World Health Organ. 2001;79(3):222–6.Google Scholar
  14. 14.
    Javitt JC, Wang F, West SK. Blindness Due to Cataract: Epidemiology and Prevention. Annu Rev Public Health [Internet]. 1996;17(1):159–77. Available from:  https://doi.org/10.1146/annurev.pu.17.050196.001111 CrossRefGoogle Scholar
  15. 15.
    Deroy O, Auvray M. Reading the world through the skin and ears: A new perspective on sensory substitution. Front Psychol. 2012;3(NOV).Google Scholar
  16. 16.
    Bach-y-Rita PW, Kercel S. Sensory substitution and the human-machine interface. Vol. 7, Trends in Cognitive Sciences. 2003. p. 541–6.Google Scholar
  17. 17.
    Capelle C, Trullemans C, Arno P, Veraart C. A real-time experimental prototype for enhancement of vision rehabilitation using auditory substitution. IEEE Trans Biomed Eng. 1998;45(10):1279–93.CrossRefGoogle Scholar
  18. 18.
    Hanneton S, Auvray M, Durette B. The Vibe: A versatile vision-to-audition sensory substitution device. Appl Bionics Biomech. 2010;7(4):269–76.CrossRefGoogle Scholar
  19. 19.
    Lenay C, Gapenne O, Hanneton S, Marque C, Genouëlle C. Sensory Substitution : Limits and Perspectives. Touching Knowing Cogn Psychol haptic Man Percept [Internet]. 2003;19:275–292. Available from: http://books.google.com/books?hl=fr&lr=&id=GSOhMpdyobAC&pgis=1CrossRefGoogle Scholar
  20. 20.
    Margalit E, Maia M, Weiland JD, Greenberg RJ, Fujii GY, Torres G, et al. Retinal prosthesis for the blind. Survey of Ophthalmology. 2002.Google Scholar
  21. 21.
    Luo YHL, da Cruz L. The Argus® II Retinal Prosthesis System. Progress in Retinal and Eye Research. 2016.Google Scholar
  22. 22.
    Ahuja AK, Dorn JD, Caspi A, McMahon MJ, Dagnelie G, DaCruz L, et al. Blind subjects implanted with the Argus II retinal prosthesis are able to improve performance in a spatial-motor task. Br J Ophthalmol. 2011Google Scholar
  23. 23.
    Luo YHL, Zhong JJ, da Cruz L. The use of Argus® II retinal prosthesis by blind subjects to achieve localisation and prehension of objects in 3-dimensional space. Graefe’s Arch Clin Exp Ophthalmol. 2015Google Scholar
  24. 24.
    Dorn JD, Ahuja AK, Caspi A, Da Cruz L, Dagnelie G, Sahel JA, et al. The detection of motion by blind subjects with the epiretinal 60-electrode (Argus II) retinal prosthesis. JAMA Ophthalmol. 2013Google Scholar
  25. 25.
    Da Cruz L, Coley BF, Dorn J, Merlini F, Filley E, Christopher P, et al. The Argus II epiretinal prosthesis system allows letter and word reading and long-term function in patients with profound vision loss. Br J Ophthalmol. 2013Google Scholar
  26. 26.
    Sahel JA, da Cruz L, Hafezi F, Stanga PE, Merlini F, Coley B, et al. Subjects Blind From Outer Retinal Dystrophies Are Able To Consistently Read Short Sentences Using The ArgusTM Ii Retinal Prosthesis System. ARVO Meet Abstr. 2011Google Scholar
  27. 27.
    Stanga P, Sahel J, Mohand-Said S, DaCruz L, Caspi A, Merlini F, et al. Face Detection using the Argus® II Retinal Prosthesis System. Invest Ophthalmol Vis Sci. 2013Google Scholar
  28. 28.
    Weiland JD, Liu W, Humayun MS. Retinal Prosthesis. Annu Rev Biomed Eng. 2005;Google Scholar
  29. 29.
    Edwards TL, Cottriall CL, Xue K, Simunovic MP, Ramsden JD, Zrenner E, et al. Assessment of the Electronic Retinal Implant Alpha AMS in Restoring Vision to Blind Patients with End-Stage Retinitis Pigmentosa. Ophthalmology. 2018Google Scholar
  30. 30.
    Stingl K, Bartz-Schmidt KU, Besch D, Braun A, Bruckmann A, Gekeler F, et al. Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS. Proc R Soc B Biol Sci. 2013Google Scholar
  31. 31.
    Zrenner E, Bruckmann A, Greppmaier U, Hoertdoerfer G, Kernstock C, Sliesoraityte I, et al. Improvement of Visual Orientation and Daily Skills Mediated by Subretinal Electronic Implant Alpha IMS in Previously Blind RP Patients. In: ARVO Meeting Abstracts. 2011.Google Scholar
  32. 32.
    Stingl K, Bartz-Schmidt KU, Besch D, Gekeler F, Greppmaier U, Hörtdörfer G, et al. What can blind patients see in daily life with the subretinal Alpha IMS implant? Current overview from the clinical trial in Tübingen. Ophthalmologe. 2012Google Scholar
  33. 33.
    Haim M. Epidemiology of retinitis pigmentosa in Denmark. Acta Ophthalmol. 2002;Google Scholar
  34. 34.
    Hu DN Prevalence and mode of inheritance of major genetic eye diseases in China. J Med Genet. 1987;Google Scholar
  35. 35.
    Gröndahl J. Tapeto-retinal degeneration in four Norwegian counties II: Diagnostic evaluation of 407 relatives and genetic evaluation of 87 families. Clin Genet. 1986Google Scholar
  36. 36.
    Bunker CH, Berson EL, Bromley WC, Hayes RP, Roderick TH. Prevalence of retinitis pigmentosa in maine. Am J Ophthalmol. 1984Google Scholar
  37. 37.
    Bundey S, Crews SJ. A study of retinitis pigmentosa in the City of Birmingham. II Clinical and genetic heterogeneity. J Med Genet. 1984Google Scholar
  38. 38.
    Ammann F, Klein D, Franceschetti A. Genetic and epidemiological investigations on pigmentary degeneration of the retina and allied disorders in Switzerland. J Neurol Sci. 1965;Google Scholar
  39. 39.
    Veraart C, Raftopoulos C, Mortimer JT, Delbeke J, Pins D, Michaux G, et al. Visual sensations produced by optic nerve stimulation using an implanted self-sizing spiral cuff electrode. Brain Res. 1998Google Scholar
  40. 40.
    Veraart C, Wanet-Defalque MC, Gérard B, Vanlierde A, Delbeke J. Pattern Recognition with the Optic Nerve Visual Prosthesis. Artif Organs. 2003Google Scholar
  41. 41.
    Marg E, Dierssen G. Reported visual percepts from stimulation of the human brain with microelectrodes during therapeutic surgery. Confinia neurologica. 1965.Google Scholar
  42. 42.
    Panetsos F, Sanchez-Jimenez A, Cerio ED De Diaz-Guemes I, Sanchez FM. Consistent phosphenes generated by electrical microstimulation of the visual thalamus. An experimental approach for thalamic visual neuroprostheses. Front Neurosci. 2011Google Scholar
  43. 43.
    Pezaris JS, Reid RC. Demonstration of artificial visual percepts generated through thalamic microstimulation. Proc Natl Acad Sci. 2007Google Scholar
  44. 44.
    Löwenstein K, Borchardt M. Symptomatologie und elektrische Reizung bei einer Schußverletzung des Hinterhauptlappens. Dtsch Z Nervenheilkd. 1918;58(3–6):264–92.CrossRefGoogle Scholar
  45. 45.
    Krause F. Die Sehbahn in Chirurgischer Beziehung und die Faradische Reizung des Sehzentrums. Klin Wochenschr. 1924;3(28):1260–5.CrossRefGoogle Scholar
  46. 46.
    Foerster O. Beitrage zur Pathophysiologie der Sehbahn und der Sehsphare. J Psychol Neurol, Lpz. 1929;39:463.Google Scholar
  47. 47.
    Brindley GS, Lewin WS. The sensations produced by electrical stimulation of the visual cortex. J Physiol. 1968;196(2):479–93.CrossRefGoogle Scholar
  48. 48.
    Dobelle WH, Mladejovsky MG. Phosphenes produced by electrical stimulation of human occipital cortex, and their application to the development of a prosthesis for the blind. J Physiol. 1974;243(2):553–76.CrossRefGoogle Scholar
  49. 49.
    Dobelle WH, Mladejovsky MG, Girvin JP. Artificial Vision for the Blind: Electrical Stimulation of Visual Cortex Offers Hope for a Functional Prosthesis. Science (80- ) [Internet]. 1974;183(4123):440–4. Available from:  https://doi.org/10.1126/science.183.4123.440
  50. 50.
    Dobelle WH, Mladejovsky MG, Evans JR, Roberts TS, Girvin JP. Braille reading by a blind volunteer by visual cortex stimulation. Nature. 1976;259(5539):111–2.CrossRefGoogle Scholar
  51. 51.
    Dobelle WH. Artificial vision for the blind by connecting a television camera to the visual cortex. ASAIO J. 2000;46(1):3–9.CrossRefGoogle Scholar
  52. 52.
    Bak M, Girvin JP, Hambrecht FT, Kufta C V., Loeb GE, Schmidt EM. Visual sensations produced by intracortical microstimulation of the human occipital cortex. Med Biol Eng Comput. 1990;28(3):257–9.CrossRefGoogle Scholar
  53. 53.
    Bartlett JR, Doty RW. An exploration of the ability of macaques to detect microstimulation of striate cortex. Acta Neurobiol Exp (Wars). 1980;40(4):713–27.Google Scholar
  54. 54.
    Schmidt EM, Bak MJ, Hambrecht FT, Kufta C V., O’Rourke DK, Vallabhanath P. Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. Brain. 1996;119(2):507–22.CrossRefGoogle Scholar
  55. 55.
    Bosking WH, Beauchamp MS, Yoshor D. Electrical Stimulation of Visual Cortex: Relevance for the Development of Visual Cortical Prosthetics. Annu Rev Vis Sci. 2017Google Scholar
  56. 56.
    Yoshor D, Bosking WH, Lega BC, Sun P, Maunsell JHR. Local cortical function after uncomplicated subdural electrode implantation. J Neurosurg. 2008;Google Scholar
  57. 57.
    Yoshor D, Bosking WH, Ghose GM, Maunsell JHR. Receptive fields in human visual cortex mapped with surface electrodes. Cereb Cortex. 2007;17(10):2293–302.CrossRefGoogle Scholar
  58. 58.
    Winawer J, Parvizi J. Linking Electrical Stimulation of Human Primary Visual Cortex, Size of Affected Cortical Area, Neuronal Responses, and Subjective Experience. Neuron. 2016;92(6):1213–9.CrossRefGoogle Scholar
  59. 59.
    Richard P, Bosking WH. Mapping of the Human Visual System. Clin Brain Mapp. 2012;219.Google Scholar
  60. 60.
    Lee HW, Hong SB, Seo DW, Tae WS, Hong SC. Mapping of functional organization in human visual cortex Electrical cortical stimulation. Neurology. 2000;54(4):849–54.CrossRefGoogle Scholar
  61. 61.
    Bosking WH, Foster B, Sun P, Beauchamp MS, Yoshor D. Rules Governing Perception of Multiple Phosphenes by Human Observers. bioRxiv. 2018;302547.Google Scholar
  62. 62.
    Bosking WH, Sun P, Ozker M, Pei X, Foster BL, Beauchamp MS, et al. Saturation in Phosphene Size with Increasing Current Levels Delivered to Human Visual Cortex. J Neurosci. 2017;Google Scholar
  63. 63.
    Troyk PR. The Intracortical Visual Prosthesis Project. In: Artificial Vision. Springer; 2017. p. 203–14.Google Scholar
  64. 64.
    Rush AD, Troyk PR. A power and data link for a wireless-implanted neural recording system. IEEE Trans Biomed Eng. 2012;59(12 PART2):3255–62.CrossRefGoogle Scholar
  65. 65.
    Kim T, Troyk PR, Bak M. Active Floating Micro Electrode Arrays (AFMA). In: Annual International Conference of the IEEE Engineering in Medicine and Biology - Proceedings. 2006.Google Scholar
  66. 66.
    Fernández E, Normann RA. CORTIVIS Approach for an Intracortical Visual Prostheses. In: Artificial Vision. Springer; 2017. p. 191–201.Google Scholar
  67. 67.
    Maynard EM, Nordhausen CT, Normann RA. The Utah Intracortical Electrode Array: A recording structure for potential brain-computer interfaces. Electroencephalogr Clin Neurophysiol. 1997;Google Scholar
  68. 68.
    Romero S, Pelayo FJ, Morillas CA, Martínez A, Fernández E. Reconfigurable Retina-Like Preprocessing Platform for Cortical Visual Neuroprostheses. In: Handbook of Neural Engineering. 2006.Google Scholar
  69. 69.
    Fernandez E, Alfaro A, Toledano R, Albisua J, García A. Perceptions elicited by electrical stimulation of human visual cortex. Invest Ophthalmol Vis Sci. 2015;56(7):777.Google Scholar
  70. 70.
    Lowery AJ, Rosenfeld J V, Rosa MGP, Brunton E, Rajan R, Mann C, et al. Monash Vision Group’s Gennaris Cortical Implant for Vision Restoration. In: Artificial Vision. Springer; 2017. p. 215–25.Google Scholar
  71. 71.
    Lowery AJ, Rosenfeld J V., Lewis PM, Browne D, Mohan A, Brunton E, et al. Restoration of vision using wireless cortical implants: The Monash Vision Group project. In: Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS. 2015.Google Scholar
  72. 72.
    Li WH, Tang TJJ, Lui WLD. Going beyond vision to improve bionic vision. In: 2013 IEEE International Conference on Image Processing, ICIP 2013 - Proceedings. 2013.Google Scholar
  73. 73.
    Wang C, Brunton E, Haghgooie S, Cassells K, Lowery A, Rajan R. Characteristics of electrode impedance and stimulation efficacy of a chronic cortical implant using novel annulus electrodes in rat motor cortex. J Neural Eng. 2013Google Scholar
  74. 74.
    da Cruz L, Dorn JD, Humayun MS, Dagnelie G, Handa J, Barale PO, et al. Five-Year Safety and Performance Results from the Argus II Retinal Prosthesis System Clinical Trial. Ophthalmology. 2016Google Scholar
  75. 75.
    Merabet LB, Rizzo JF, Pascual-Leone A, Fernandez E. “Who is the ideal candidate?” Decisions and issues relating to visual neuroprosthesis development, patient testing and neuroplasticity. J Neural Eng. 2007Google Scholar
  76. 76.
    Stingl K, Bartz-Schmidt KU, Besch D, Chee CK, Cottriall CL, Gekeler F, et al. Subretinal Visual Implant Alpha IMS - Clinical trial interim report. Vision Res. 2015Google Scholar
  77. 77.
    Liu X, McCreery DB, Bullara LA, Agnew WF. Evaluation of the stability of intracortical microelectrode arrays. IEEE Trans Neural Syst Rehabil Eng. 2006Google Scholar
  78. 78.
    Jorfi M, Skousen JL, Weder C, Capadona JR. Progress towards biocompatible intracortical microelectrodes for neural interfacing applications. Journal of Neural Engineering. 2015.Google Scholar
  79. 79.
    Schwartz AB, Cui XT, Weber DJJ, Moran DW. Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics. Neuron. 2006.Google Scholar
  80. 80.
    Goss-Varley M, Dona KR, McMahon JA, Shoffstall AJ, Ereifej ES, Lindner SC, et al. Microelectrode implantation in motor cortex causes fine motor deficit: Implications on potential considerations to Brain Computer Interfacing and Human Augmentation. Sci Rep. 2017;Google Scholar
  81. 81.
    Biran R, Martin DC, Tresco PA. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol. 2005;Google Scholar
  82. 82.
    Potter KA, Buck AC, Self WK, Capadona JR. Stab injury and device implantation within the brain results in inversely multiphasic neuroinflammatory and neurodegenerative responses. J Neural Eng. 2012;Google Scholar
  83. 83.
    Kipke DR, Shain W, Buzsaki G, Fetz E, Henderson JM, Hetke JF, et al. Advanced Neurotechnologies for Chronic Neural Interfaces: New Horizons and Clinical Opportunities. J Neurosci. 2008;Google Scholar
  84. 84.
    Margalit E, Weiland JD, Clatterbuck RE, Fujii GY, Maia M, Tameesh M, et al. Visual and electrical evoked response recorded from subdural electrodes implanted above the visual cortex in normal dogs under two methods of anesthesia. J Neurosci Methods. 2003;Google Scholar
  85. 85.
    Thompson MC, Herron JA, Brown T, Ojemann JG, Ko AL, Chizeck HJ. Demonstration of a stable chronic electrocorticography-based brain-computer interface using a deep brain stimulator. In: 2016 IEEE International Conference on Systems, Man, and Cybernetics, SMC 2016 - Conference Proceedings. 2017.Google Scholar
  86. 86.
    Leuthardt EC, Schalk G, Wolpaw JR, Ojemann JG, Moran DW. A brain-computer interface using electrocorticographic signals in humans. J Neural Eng. 2004;Google Scholar
  87. 87.
    Nair DR, Burgess R, McIntyre CC, Lüders H. Chronic subdural electrodes in the management of epilepsy. Clinical Neurophysiology. 2008.Google Scholar
  88. 88.
    Wyler AR, Ojemann GA, Lettich E, Ward AA. Subdural strip electrodes for localizing epileptogenic foci. J Neurosurg. 1984;Google Scholar
  89. 89.
    Wandell BA, Dumoulin SO, Brewer AA. Visual field maps in human cortex. Neuron. 2007.Google Scholar
  90. 90.
    Schaeffner LF, Welchman AE. Mapping the visual brain areas susceptible to phosphene induction through brain stimulation. Exp Brain Res. 2017;Google Scholar
  91. 91.
    Benson NC, Butt OH, Brainard DH, Aguirre GK. Correction of Distortion in Flattened Representations of the Cortical Surface Allows Prediction of V1-V3 Functional Organization from Anatomy. PLoS Comput Biol. 2014;Google Scholar
  92. 92.
    Dobelle WH, Quest DO, Antunes JL, Roberts TS, Girvin JP. Artificial vision for the blind by electrical stimulation of the visual cortex. Neurosurgery. 1979;5(4):521–7.CrossRefGoogle Scholar
  93. 93.
    Dagnelie G. Psychophysical Evaluation for Visual Prosthesis. Annu Rev Biomed Eng. 2008;Google Scholar
  94. 94.
    Shannon R V. A Model of Safe Levels for Electrical Stimulation. IEEE Trans Biomed Eng. 1992;39(4):424–6.CrossRefGoogle Scholar
  95. 95.
    Merrill DR, Bikson M, Jefferys JGR. Electrical stimulation of excitable tissue: Design of efficacious and safe protocols. Vol. 141, Journal of Neuroscience Methods. 2005. p. 171–98.Google Scholar
  96. 96.
    Arathorn DW, Stevenson SB, Yang Q, Tiruveedhula P, Roorda A. How the unstable eye sees a stable and moving world. J Vis. 2013;Google Scholar
  97. 97.
    Ghuman AS, Brunet NM, Li Y, Konecky RO, Pyles JA, Walls SA, et al. Dynamic encoding of face information in the human fusiform gyrus. Nat Commun. 2014;Google Scholar
  98. 98.
    Liu H, Agam Y, Madsen JR, Kreiman G. Timing, Timing, Timing: Fast Decoding of Object Information from Intracranial Field Potentials in Human Visual Cortex. Neuron. 2009;Google Scholar
  99. 99.
    Kapeller C, Ogawa H, Schalk G, Kunii N, Coon WG, Scharinger J, et al. Real-time detection and discrimination of visual perception using electrocorticographic signals. J Neural Eng. 2018;Google Scholar
  100. 100.
    Aminoff EM, Li Y, Pyles JA, Ward MJ, Richardson RM, Ghuman AS. Associative hallucinations result from stimulating left ventromedial temporal cortex. Cortex. 2016;Google Scholar
  101. 101.
    Blanke O, Landis T, Seeck M. Electrical cortical stimulation of the human prefrontal cortex evokes complex visual hallucinations. Epilepsy Behav. 2000Google Scholar
  102. 102.
    Penfield W, Rasmussen T. The Cerebral Cortex of Man. A Clinical Study of Localization of Function.pdf. Academic Medicine. 1950.Google Scholar
  103. 103.
    Rangarajan V, Hermes D, Foster BL, Weiner KS, Jacques C, Grill-Spector K, et al. Electrical Stimulation of the Left and Right Human Fusiform Gyrus Causes Different Effects in Conscious Face Perception. J Neurosci. 2014;Google Scholar
  104. 104.
    Parvizi J, Jacques C, Foster BL, Withoft N, Rangarajan V, Weiner KS, et al. Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception. J Neurosci. 2012;Google Scholar
  105. 105.
    Mani J, Diehl B, Piao Z, Schuele SS, Lapresto E, Liu P, et al. Evidence for a basal temporal visual language center: Cortical stimulation producing pure alexia. Neurology. 2008;Google Scholar
  106. 106.
    Hirshorn EA, Li Y, Ward MJ, Richardson RM, Fiez JA, Ghuman AS. Decoding and disrupting left midfusiform gyrus activity during word reading. Proc Natl Acad Sci. 2016;Google Scholar
  107. 107.
    Kravitz DJ, Saleem KS, Baker CI, Ungerleider LG, Mishkin M. The ventral visual pathway: An expanded neural framework for the processing of object quality. Trends in Cognitive Sciences. 2013.Google Scholar
  108. 108.
    Kravitz DJ, Saleem KS, Baker CI, Mishkin M. A new neural framework for visuospatial processing. Nature Reviews Neuroscience. 2011.Google Scholar

Copyright information

© The American Society for Experimental NeuroTherapeutics, Inc. 2018

Authors and Affiliations

  1. 1.Department of BioengineeringUniversity of California Los AngelesLos AngelesUSA
  2. 2.Department of NeurosurgeryUniversity of California Los AngelesLos AngelesUSA

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