Plasticity of the human visual system after retinal gene therapy in patients with Leber's congenital amaurosis

Science Translational Medicine

Volumn 7, Issue 296, 2015, Pages

  Ashtari, Manzar ^a,b   Zhang, Hui ^c   Cook, Philip A ^d   Cyckowski, Laura L ^e   Shindler, Kenneth S ^a,b   Marshall, Kathleen A ^e   Aravand, Puya ^a,b   Vossough, Arastoo ^e   Gee, James C ^d   Maguire, Albert M ^a,b,e   Baker, Chris I ^f   Bennett, Jean ^a,b,e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINAL PIGMENT EPITHELIUM SPECIFIC PROTEIN 65; UNCLASSIFIED DRUG; VISUAL PROTEINS AND PIGMENTS;

ADENO ASSOCIATED VIRUS 2; ADOLESCENT; ADULT; AGE; ARTICLE; CHILD; CLINICAL ARTICLE; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; FEMALE; FRACTIONAL ANISOTROPY; GENE MUTATION; GENE VECTOR; GENICULATE BODY; HUMAN; LEBER CONGENITAL AMAUROSIS; MALE; NERVE CELL PLASTICITY; NEUROIMAGING; NON INVASIVE PROCEDURE; NUCLEAR MAGNETIC RESONANCE IMAGING; NYSTAGMUS; PRIORITY JOURNAL; RETINA; RPE65 GENE; STRIATE CORTEX; TREATMENT OUTCOME; VIRAL GENE THERAPY; VISUAL SYSTEM; VOXEL BASED MORPHOMETRY; WHITE MATTER; ANISOTROPY; CASE CONTROL STUDY; DIFFUSION TENSOR IMAGING; GENE THERAPY; GENETICS; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; VISION; VISUAL CORTEX; YOUNG ADULT;

ADOLESCENT; ADULT; ANISOTROPY; CASE-CONTROL STUDIES; CHILD; DIFFUSION TENSOR IMAGING; FEMALE; GENETIC THERAPY; GENETIC VECTORS; HUMANS; LEBER CONGENITAL AMAUROSIS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROIMAGING; NEURONAL PLASTICITY; RETINA; VISION, OCULAR; VISUAL CORTEX; YOUNG ADULT;

EID: 84937132298     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa8791     Document Type: Article

References (56)

1. N. Sadato, A. Pascual-Leone, J. Grafman, V. Ibañez, M. P. Deiber, G. Dold, M. Hallett, Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380, 526-528 (1996).
2. H. Burton, A. Z. Snyder, J. B. Diamond, M. E. Raichle, Adaptive changes in early and late blind: A fMRI study of verb generation to heard nouns. J. Neurophysiol. 88, 3359-3371 (2002).
3. I. Fine, A. R. Wade, A. A. Brewer, M. G. May, D. F. Goodman, G. M. Boynton, B. A. Wandell, D. I. MacLeod, Long-term deprivation affects visual perception and cortex. Nat. Neurosci. 6, 915-916 (2003).
4. A. Valvo, L. L. Clark, Z. S. Jastrzembska, Sight Restoration After Long Term Blindness: The Problems and Behavior Patterns of Visual Rehabilitation (American Foundation for the Blind, New York, 1971).
5. F. Valverde, Apical dendritic spines of the visual cortex and light deprivation in the mouse. Exp. Brain Res. 3, 337-352 (1967).
6. S. Borges, M. Berry, The effects of dark rearing on the development of the visual cortex of the rat. J. Comp. Neurol. 180, 277-300 (1978).
7. D. H. Hubel, T. N. Wiesel, Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106-154 (1962)
8. A. Antonini, M. P. Stryker, Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci. 13, 3549-3573 (1993).
9. A. Antonini, M. Fagiolini, M. P. Stryker, Anatomical correlates of functional plasticity in mouse visual cortex. J. Neurosci. 19, 4388-4406 (1999).
10. H. Yu, A. K. Majewska, M. Sur, Rapid experience-dependent plasticity of synapse function and structure in ferret visual cortex in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, 21235-21240 (2011).
11. T. N. Wiesel, D. H. Hubel, Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003-1017 (1963).
12. J. S. Shimony, H. Burton, A. A. Epstein, D. G. McLaren, S. W. Sun, A. Z. Snyder, Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb. Cortex 16, 1653-1661 (2006).
13. C. Yu, N. Shu, J. Li, W. Qin, T. Jiang, K. Li, Plasticity of the corticospinal tract in early blindness revealed by quantitative analysis of fractional anisotropy based on diffusion tensor tractography. Neuroimage 36,411-417 (2007).
14. N. Leporé, P. Voss, F. Lepore, Y.-Y. Chou, M. Fortin, F. Gougoux, A. D. Lee, C. Brun, M. Lassonde, S. K. Madsen, A. W. Toga, P. M. Thompson, Brain structure changes visualized in early- and late-onset blind subjects. Neuroimage 49, 134-140 (2010).
15. M. R. Dürsteler, L. J. Garey, J. A. Movshon, Reversal of the morphological effects of monocular deprivation in the kittens's lateral geniculate nucleus. J. Physiol. 261, 189-210 (1976).
16. S. LeVay, T. N. Wiesel, D. H. Hubel, The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191, 1-51 (1980).
17. N. V. Swindale, F. Vital-Durand, C. Blakemore, Recovery from monocular deprivation in the monkey. III. Reversal of anatomical effects in the visual cortex. Proc. R. Soc. Lond. Ser. B 213, 435-450 (1981).
18. J. A. Movshon, Reversal of the physiological effects of monocular deprivation in the kitten's visual cortex. J. Physiol. 261, 125-174 (1976).
19. M. Ashtari, L. L. Cyckowski, J. F. Monroe, K. A. Marshall, D. C. Chung, A. Auricchio, F. Simonelli, B. P. Leroy, A. M. Maguire, K. S. Shindler, J. Bennett, The human visual cortex responds to gene therapy-mediated recovery of retinal function. J. Clin. Invest. 121, 2160-2168 (2011).
20. R. F. Dougherty, M. Ben-Shachar, R. Bammer, A. A. Brewer, B. A. Wandell, Functional organization of human occipital-callosal fiber tracts. Proc. Natl. Acad. Sci. U.S.A. 102,7350-7355 (2005).
21. S.-K. Song, J. Yoshino, T. Q. Le, S.-J. Lin, S.-W. Sun, A. H. Cross, R. C. Armstrong, Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140 (2005).
22. J. M. Tyszka, C. Readhead, E. L. Bearer, R. G. Pautler, R. E. Jacobs, Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 29, 1058-1065 (2006).
23. N. Shu, Y. Liu, J. Li, Y. Li, C. Yu, T. Jiang, Altered anatomical network in early blindness revealed by diffusion tensor tractography. PLOS One 4, e7228 (2009).
24. U. Noppeney, K. J. Friston, J. Ashburner, R. Frackowiak, C. J. Price, Early visual deprivation induces structural plasticity in gray and white matter. Curr. Biol. 15, R488-R490 (2005).
25. M. Ptito, F. C. Schneider, O. B. Paulson, R. Kupers, Alterations of the visual pathways in congenital blindness. Exp. Brain Res. 187, 41-49 (2008).
26. L. A. Yannuzzi, Central serous chorioretinopathy: A personal perspective. Am. J. Ophthalmol. 149, 361-363 (2010).
27. D. C. Chung, E. I. Traboulsi, Leber congenital amaurosis: Clinical correlations with genotypes, gene therapy trials update, and future directions. J. AAPOS 13, 587-592 (2009).
28. I. Perrault, J. M. Rozet, S. Gerber, I. Ghazi, C. Leowski, D. Ducroq, E. Souied, J. L. Dufier, A. Munnich, J. Kaplan, Leber congenital amaurosis. Mol. Genet. Metab. 68, 200-208 (1999).
29. K. Al-Khayer, S. Hagstrom, G. Pauer, H. Zegarra, J. Sears, E. I. Traboulsi, Thirty-year follow-up of a patient with leber congenital amaurosis and novel RPE65 mutations. Am. J. Ophthalmol. 137, 375-377 (2004).
30. D. H. Salat, E. E. Smith, D. S. Tuch, T. Benner, V. Pappu, K. M. Schwab, M. E. Gurol, H. D. Rosas, J. Rosand, S. M. Greenberg, White matter alterations in cerebral amyloid angiopathy measured by diffusion tensor imaging. Stroke 37, 1759-1764 (2006).
31. C. Davatzikos, S. M. Resnick, Degenerative age changes in white matter connectivity visualized in vivo using magnetic resonance imaging. Cereb. Cortex 12, 767-771 (2002).
32. P. Kochunov, D. E. Williamson, J. Lancaster, P. Fox, J. Cornell, J. Blangero, D. C. Glahn, Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiol. Aging 33, 9-20 (2012).
33. J. H. Steiger, Tests for comparing elements of a correlation matrix. Psychol. Bull. 87, 245-251 (1980).
34. J. Bennett, M. Ashtari, J. Wellman, K. A. Marshall, L. L. Cyckowski, D. C. Chung, S. McCague, E. A. Pierce, Y. Chen, J. L. Bennicelli, X. Zhu, G. S. Ying, J. Sun, J. F. Wright, A. Auricchio, F. Simonelli, K. S. Shindler, F. Mingozzi, K. A. High, A. M. Maguire, AAV2 gene therapy readministration in three adults with congenital blindness. Sci. Transl. Med. 4, 120ra115 (2012).
35. R. W. Hertle, L. F. Dell'Osso, Nystagmus in Infancy and Childhood: Current Concepts in Mechanisms, Diagnoses, and Management (Oxford Univ. Press, New York, 2013).
36. D. H. Hubel, T. N. Wiesel, The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206, 419-436 (1970).
37. W. J. Pan, G. Wu, C. X. Li, F. Lin, J. Sun, H. Lei, Progressive atrophy in the optic pathway and visual cortex of early blind Chinese adults: A voxel-based morphometry magnetic resonance imaging study. Neuroimage 37, 212-220 (2007).
38. D. A. Paul, E. Gaffin-Cahn, E. B. Hintz, G. J. Adeclat, T. Zhu, Z. R. Williams, G. E. Vates, B. Z. Mahon, White matter changes linked to visual recovery after nerve decompression. Sci. Transl. Med. 6, 266ra173 (2014).
39. R. D. Fields, White matter in learning, cognition and psychiatric disorders. Trends Neurosci. 31, 361-370 (2008).
40. T. Ishibashi, K. A. Dakin, B. Stevens, P. R. Lee, S. V. Kozlov, C. L. Stewart, R. D. Fields, Astrocytes promote myelination in response to electrical impulses. Neuron 49,823-832 (2006).
41. Y. Kozorovitskiy, C. G. Gross, C. Kopil, L. Battaglia, M. McBreen, A. M. Stranahan, E. Gould, Experience induces structural and biochemical changes in the adult primate brain. Proc. Natl. Acad. Sci. U.S.A. 102, 17478-17482 (2005).
42. S. L. Bengtsson, Z. Nagy, S. Skare, L. Forsman, H. Forssberg, F. Ullén, Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 8, 1148-1150 (2005).
43. J. Scholz, M. C. Klein, T. E. Behrens, H. Johansen-Berg, Training induces changes in white-matter architecture. Nat. Neurosci. 12, 1370-1371 (2009).
44. M. Taubert, B. Draganski, A. Anwander, K. Müller, A. Horstmann, A. Villringer, P. Ragert, Dynamic properties of human brain structure: Learning-related changes in cortical areas and associated fiber connections. J. Neurosci. 30, 11670-11677 (2010).
45. E. M. Stone, Leber congenital amaurosis - A model for efficient genetic testing of heterogeneous disorders: LXIV Edward Jackson memorial lecture. Am. J. Ophthalmol. 144, 791-811 (2007).
46. A. M. Maguire, F. Simonelli, E. A. Pierce, E. N. Pugh Jr., F. Mingozzi, J. Bennicelli, S. Banfi, K. A. Marshall, F. Testa, E. M. Surace, S. Rossi, A. Lyubarsky, V. R. Arruda, B. Konkle, E. Stone, J. Sun, J. Jacobs, L. Dell'Osso, R. Hertle, J.-X. Ma, T. M. Redmond, X. Zhu, B. Hauck, O. Zelenaia, K. S. Shindler, M. G. Maguire, J. F. Wright, N. J. Volpe, J. W. McDonnell, A. Auricchio, K. A. High, J. Bennett, Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358, 2240-2248 (2008).
47. A. M. Maguire, K. A. High, A. Auricchio, J. F. Wright, E. A. Pierce, F. Testa, F. Mingozzi, J. L. Bennicelli, G. S. Ying, S. Rossi, A. Fulton, K. A. Marshall, S. Banfi, D. C. Chung, J. I. Morgan, B. Hauck, O. Zelenaia, X. Zhu, L. Raffini, F. Coppieters, E. De Baere, K. S. Shindler, N. J. Volpe, E. M. Surace, C. Acerra, A. Lyubarsky, T. M. Redmond, E. Stone, J. Sun, J. W. McDonnell, B. P. Leroy, F. Simonelli, J. Bennett, Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: A phase 1 dose-escalation trial. Lancet 374, 1597-1605 (2009).
48. C. Pierpaoli, P. J. Basser, Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 36, 893-906 (1996).
49. T. E. Nichols, A. P. Holmes, Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum. Brain Mapp. 15, 1-25 (2002).
50. E. Brunner, U. Munzel, The nonparametric Behrens-Fisher problem: Asymptotic theory and a small-sample approximation. Biom. J. 42,17-25 (2000).
51. H. Zhang, P. A. Yushkevich, D. C. Alexander, J. C. Gee, Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10,764-785 (2006).
52. H. Zhang, P. A. Yushkevich, D. Rueckert, J. C. Gee, Unbiased white matter atlas construction using diffusion tensor images. Med. Image Comput. Comput. Assist. Interv. 10, 211-218 (2007).
53. S. Mori, W. E. Kaufmann, C. Davatzikos, B. Stieltjes, L. Amodei, K. Fredericksen, G. D. Pearlson, E. R. Melhem, M. Solaiyappan, G. V. Raymond, H. W. Moser, P. C. van Zijl, Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn. Reson. Med. 47, 215-223 (2002).
54. T. Okada, Y. Miki, Y. Fushimi, T. Hanakawa, M. Kanagaki, A. Yamamoto, S. Urayama, H. Fukuyama, M. Hiraoka, K. Togashi, Diffusion-tensor fiber tractography: Intraindividual comparison of 3.0-T and 1.5-T MR imaging. Radiology 238,668-678 (2006).
55. S. Wakana, H. Jiang, L. M. Nagae-Poetscher, P. C. van Zijl, S. Mori, Fiber tract-based atlas of human white matter anatomy. Radiology 230, 77-87 (2004).
56. M. Ashtari, L. Cyckowski, A. Yazdi, A. Viands, K. Marshall, I. Bókkon, A. Maguire, J. Bennett, fMRI of retina-originated phosphenes experienced by patients with Leber congenital amaurosis. PLOS One 9, e86068 (2014).