The Pupil light reflex in leber's hereditary optic neuropathy: Evidence for preservation of melanopsin- expressing retinal ganglion cells

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 7, 2013, Pages 4471-4477

  Moura, Ana Laura A ^a   Nagy, Balázs V ^a,b   la Morgia, Chiara ^c,d   Barboni, Piero ^d,e   Oliveira, André Gustavo Fernandes ^a   Salomaõ, Solange R ^f   Berezovsky, Adriana ^f   de Moraes Filho, Milton Nunes ^f   Chicani, Carlos Filipe ^g   Belfort, Rubens ^f   Carelli, Valerio ^c,d   Sadun, Alfredo A ^g   Hood, Donald C ^h   Ventura, Dora Fix ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b BUDAPEST UNIVERSITY OF TECHNOLOGY AND ECONOMICS   (Hungary)

^c IRCCS ISTITUTO DELLE SCIENZE NEUROLOGICHE DI BOLOGNA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e Studio Oculistico d'Azeglio   (Italy)

^f FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^g UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^h Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Ganglion cells; LHON; Melanopsin; OCT; Pupillometry

Indexed keywords

MELANOPSIN;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HUMAN; LEBER HEREDITARY OPTIC NEUROPATHY; LUMINANCE; MALE; MOVEMENT PERCEPTION; OPTIC DISK; OPTIC NERVE ATROPHY; OPTICAL COHERENCE TOMOGRAPHY; OPTICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUPIL REFLEX; PUPILLOMETRY; RETINA GANGLION CELL; RETINAL NERVE FIBER LAYER THICKNESS; VISUAL ACUITY; VISUAL FIELD DEFECT; VISUAL IMPAIRMENT; VISUAL STIMULATION;

EID: 84879626121     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-11137     Document Type: Article

References (33)

1. Thompson HS, Montague P, Cox TA, Corbett JJ. The relationship between visual acuity, pupillary defect, and visual field loss. Am J Ophthalmol. 1982;93:681-688.
2. Kardon RH, Haupert CL, Thompson HS. The relationship between static perimetry and the relative afferent pupillary defect. Am J Ophthalmol. 1993;115:351-356.
3. Lagreze WD, Kardon RH. Correlation of relative afferent pupillary defect and estimated retinal ganglion cell loss. Graefes Arch Clin Exp Ophthalmol. 1998;236:401-404.
4. Kerrison JB, Buchanan K, Rosenberg ML, et al. Quantification of optic nerve axon loss associated with a relative afferent pupillary defect in the monkey. Arch Ophthalmol. 2001;119: 1333-1341.
5. Bergamin O, Kardon, RH. Greater pupillary escape differentiates central from peripheral visual field loss. Ophthalmology. 2002;109:771-780.
6. Wakakura M, Yokoe J. Evidence for preserved direct pupil light response in Leber's hereditary optic neuropathy. Br J Ophthalmol. 1995;79:442-446.
7. Bremner FD, Shallo-Hoffmann J, Riordan-Eva P, Smith SE. Comparing pupil function with visual function in patients with Leber's hereditary optic neuropathy. Invest Ophthalmol Vis Sci. 1999;40:2528-2534.
8. Bremner FD, Tomlin EA, Shallo-Hoffmann J, Votruba M, Smith SE. The pupil in dominant optic atrophy. Invest Ophthalmol Vis Sci. 2001;42:675-678.
9. Perganta G, Barnard AR, Katti C, et al. Non-image-forming light driven functions are preserved in a mouse model of autosomal dominant optic atrophy. PLoS One. 2013;8:e56350.
10. Wallace DC, Singh G, Lott MT, et al. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science. 1988;9;242:1427-1430.
11. Carelli V, Ross-Cisneros FN, Sadun AA. Mitochondrial dysfunction as a cause of optic neuropathies. Prog Retin Eye Res. 2004;23:53-89.
12. Jacobson DM, Stone EM, Miller NR, et al. Relative afferent pupillary defects in patients with Leber hereditary optic neuropathy and unilateral visual loss. Am J Ophthalmol. 1998; 126:291-295.
13. L̈udke H, Constantin K, Leo-Kottler B, Wilhelm H. Pupillary light reflexes in patients with Leber's hereditary optic neuropathy. Graefes Arch Clin Exp Ophthalmol. 1999;237: 207-11.
14. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci. 2000;15;20:600-605.
15. Dacey DM, Liao H, Peterson BB, et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005;17;433:749-754.
16. Gamlin PD, McDougal DH, Pokorny J, Smith VC, Yau KW, Dacey DM. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res. 2007; 47:946-954.
17. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsincontaining retinal ganglion cells: architecture, projections and intrinsic photosensitivity. Science. 2002;8;295:1065-1070.
18. G̈uler AD, Ecker JL, Lall GS, et al. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature. 2008;453:102-105.
19. Bose S, Dhillon N, Ross-Cisneros FN, Carelli V. Relative postmortem sparing of afferent pupil fibers in a patient with 3460 Leber's hereditary optic neuropathy. Graefes Arch Clin Exp Ophthalmol. 2005;243:1175-1179.
20. La Morgia C, Ross-Cisneros FN, Sadun AA, et al. Melanopsin retinal ganglion cells are resistant to neurodegeneration in mitochondrial optic neuropathies. Brain. 2010;133:2426-2438.
21. Kawasaki A, Kardon RH. Intrinsically photosensitive retinal ganglion cells. J Neuroophthalmol. 2007;27:195-204.
22. Park JC, Moura AL, Raza AS, Rhee DW, Kardon RH, Hood DC. Toward a clinical protocol for assessing rod, cone, and melanopsin contributions to the human pupil response. Invest Ophthalmol Vis Sci. 2011;52:6624-6635.
23. Sadun AA, Carelli V, Salomao SR, et al. A very large Brazilian pedigree with 11778 Leber's hereditary optic neuropathy. Trans Am Ophthalmol Soc. 2002;100:169-178.
24. Kardon R, Anderson SC, Damarjian TG, Grace EM, Stone E, Kawasaki A. Chromatic pupil responses: preferential activation of the melanopsin-mediated versus outer photoreceptormediated pupil light reflex. Ophthalmology. 2009;116:1564-1573.
25. Kardon R, Anderson SC, Damarjian TG, Grace EM, Stone E, Kawasaki A. Chromatic pupillometry in patients with retinitis pigmentosa. Ophthalmology. 2011;118:376-381.
26. Barboni P, Savini G, Valentino ML, et al. Retinal nerve fiber layer evaluation by optical coherence tomography in Leber's hereditary optic neuropathy. Ophthalmology. 2005;112:120-126.
27. Sihota R, Sony P, Gupta V, Dada T, Singh R. Diagnostic capability of optical coherence tomography in evaluating the degree of glaucomatous retinal nerve fiber damage. Invest Ophthalmol Vis Sci. 2006;47:2006-2010.
28. Hood DC, Kardon RH. A framework for comparing structural and functional measures of glaucomatous damage. Prog Retin Eye Res. 2007;26:688-710.
29. Kawasaki A, Herbst K, Sander B, Milea D. Selective wavelength pupillometry in Leber hereditary optic neuropathy. Clin Experiment Ophthalmol. 2010;38:322-324.
30. Hannibal J, Hindersson P, Ostergaard J, et al. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Invest Ophthalmol Vis Sci. 2004;45:4202-4209.
31. Nakanishi Y, Nakamura M, Tatsumi Y, Nagai-Kusuhara A, Negi A. Quantification of retinal nerve fiber layer thickness reduction associated with a relative afferent pupillary defect. Graefes Arch Clin Exp Ophthalmol. 2006;244:1480-1484.
32. Feigl B, Mattes D, Thomas R, Zele AJ. Intrinsically photosensitive (melanopsin) retinal ganglion cell function in glaucoma. Invest Ophthalmol Vis Sci. 2011;52:4362-4367.
33. Kankipati L, Girkin CA, Gamlin PD. The post-illumination pupil response is reduced in glaucoma patients. Invest Ophthalmol Vis Sci. 2011;52:2287-2292.