A positive association between intrinsically photosensitive retinal ganglion cells and retinal nerve fiber layer thinning in glaucoma

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 12, 2014, Pages 7997-8005

  Gracitelli, Carolina Pelegrini Barbosa ^a   Duque Chica, Gloria L ^b   Moura, Ana Laura ^a,b   Nagy, Balazs V ^b   de Melo, Geraldine R ^a   Roizenblatt, Marina ^a   Borba, Paula D ^a   Teixeira, Sérgio H ^a   Ventura, Dora F ^b   Paranhos, Augusto ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Glaucoma; Intrinsically photosensitive retinal ganglion cells; Non image forming visual functions; Pupil light reflex; Retinal ganglion cells

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EYE TRACKING; FEMALE; GLAUCOMA; HUMAN; MALE; OPEN ANGLE GLAUCOMA; OPTICAL COHERENCE TOMOGRAPHY; PERIMETRY; PHOTOSENSITIVITY; PHOTOSTIMULATION; PROSPECTIVE STUDY; PUPIL; PUPIL REFLEX; RETINA CONE; RETINA GANGLION CELL; RETINA NERVE CELL; RETINA ROD; RETINAL NERVE FIBER LAYER THICKNESS; VISUAL ACUITY; AGED; CASE CONTROL STUDY; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; VISUAL FIELD;

AGED; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; GLAUCOMA, OPEN-ANGLE; HUMANS; MALE; MIDDLE AGED; PHOTIC STIMULATION; PROSPECTIVE STUDIES; PUPIL; RETINAL GANGLION CELLS; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL FIELD TESTS; VISUAL FIELDS;

EID: 84916896922     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-15146     Document Type: Article

References (53)

1. Weinreb RN, Aung T, Medeiros FA. The pathophysiology and treatment of glaucoma: a review. JAMA. 2014; 311: 1901-1911.
2. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006; 90: 262-267.
3. Weinreb RN, Khaw PT. Primary open-angle glaucoma. Lancet. 2004; 363: 1711-1720.
4. Li RS, Chen BY, Tay DK, Chan HH, Pu ML, So KF. Melanopsinexpressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol Vis Sci. 2006; 47: 2951-2958.
5. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci. 2000; 20: 600-605.
6. Jean-Louis G, Zizi F, Lazzaro DR, Wolintz AH. Circadian rhythm dysfunction in glaucoma: a hypothesis. J Circadian Rhythms. 2008; 6: 1.
7. Moura AL, Nagy BV, La Morgia C, et al. The pupil light reflex in Leber's hereditary optic neuropathy: evidence for preservation of melanopsin-expressing retinal ganglion cells. Invest Ophthalmol Vis Sci. 2013; 54: 4471-4477.
8. La Morgia C, Ross-Cisneros FN, Hannibal J, Montagna P, Sadun AA, Carelli V. Melanopsin-expressing retinal ganglion cells: implications for human diseases. Vision Res. 2011; 51: 296-302.
9. Lucas RJ, Douglas RH, Foster RG. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 2001; 4: 621-626.
10. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsincontaining retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002; 295: 1065-1070.
11. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002; 295: 1070-1073.
12. Gooley JJ, Lu J, Fischer D, Saper CB. A broad role for melanopsin in nonvisual photoreception. J Neurosci. 2003; 23: 7093-7106.
13. Dacey DM, Liao HW, Peterson BB, et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005; 433: 749-754.
14. Do MT, Yau KW. Intrinsically photosensitive retinal ganglion cells. Physiol Rev. 2010; 90: 1547-1581.
15. Chen SK, Badea TC, Hattar S. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature. 2011; 476: 92-95.
16. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003; 299: 245-247.
17. 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.
18. Kawasaki A, Kardon RH. Intrinsically photosensitive retinal ganglion cells. J Neuroophthalmol. 2007; 27: 195-204.
19. Zaidi FH, Hull JT, Peirson SN, et al. Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr Biol. 2007; 17: 2122-2128.
20. LeGates TA, Altimus CM, Wang H, et al. Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature. 2012; 491: 594-598.
21. Fu Y, Zhong H, Wang MH, et al. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc Natl Acad Sci U S A. 2005; 102: 10339-10344.
22. Kankipati L, Girkin CA, Gamlin PD. The post-illumination pupil response is reduced in glaucoma patients. Invest Ophthalmol Vis Sci. 2011; 52: 2287-2292.
23. 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.
24. Chylack LT Jr, Wolfe JK, Singer DM, et al. The Lens Opacities Classification System III. The Longitudinal Study of Cataract Study Group. Arch Ophthalmol. 1993; 111: 831-836.
25. Kimura R, Levene RZ. Gonioscopic differences between primary open-angle glaucoma and normal subjects over 40 years of age. Am J Ophthalmol. 1975; 80: 56-61.
26. Hillman JS. Acute closed-angle glaucoma: an investigation into the effect of delay in treatment. Br J Ophthalmol. 1979; 63: 817-821.
27. Mills RP, Budenz DL, Lee PP, et al. Categorizing the stage of glaucoma from pre-diagnosis to end-stage disease. Am J Ophthalmol. 2006; 141: 24-30.
28. 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.
29. Kardon R, Anderson SC, Damarjian TG, Grace EM, Stone E, Kawasaki A. Chromatic pupillometry in patients with retinitis pigmentosa. Ophthalmology. 2011; 118: 376-381.
30. 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.
31. Spaeth GL, Henderer J, Liu C, et al. The disc damage likelihood scale: reproducibility of a new method of estimating the amount of optic nerve damage caused by glaucoma. Trans Am Ophthalmol Soc. 2002; 100: 181-185. discussion 185-186.
32. Murdoch IE, Morris SS, Cousens SN. People and eyes: statistical approaches in ophthalmology. Br J Ophthalmol. 1998; 82: 971-973.
33. Harwerth RS, Carter-Dawson L, Smith EL III, Barnes G, Holt WF, Crawford ML. Neural losses correlated with visual losses in clinical perimetry. Invest Ophthalmol Vis Sci. 2004; 45: 3152-3160.
34. Hood DC, Kardon RH. A framework for comparing structural and functional measures of glaucomatous damage. Prog Retin Eye Res. 2007; 26: 688-710.
35. Medeiros FA, Alencar LM, Zangwill LM, Bowd C, Sample PA, Weinreb RN. Prediction of functional loss in glaucoma from progressive optic disc damage. Arch Ophthalmol. 2009; 127: 1250-1256.
36. Quigley HA, Dunkelberger GR, Green WR. Retinal ganglion cell atrophy correlated with automated perimetry in human eyes with glaucoma. Am J Ophthalmol. 1989; 107: 453-464.
37. Kerrigan-Baumrind LA, Quigley HA, Pease ME, Kerrigan DF, Mitchell RS. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest Ophthalmol Vis Sci. 2000; 41: 741-748.
38. Shou T, Liu J, Wang W, Zhou Y, Zhao K. Differential dendritic shrinkage of alpha and beta retinal ganglion cells in cats with chronic glaucoma. Invest Ophthalmol Vis Sci. 2003; 44: 3005-3010.
39. Quigley HA, Dunkelberger GR, Green WR. Chronic human glaucoma causing selectively greater loss of large optic nerve fibers. Ophthalmology. 1988; 95: 357-363.
40. Glovinsky Y, Quigley HA, Dunkelberger GR. Retinal ganglion cell loss is size dependent in experimental glaucoma. Invest Ophthalmol Vis Sci. 1991; 32: 484-491.
41. Chew SS, Cunnningham WJ, Gamble GD, Danesh-Meyer HV. Retinal nerve fiber layer loss in glaucoma patients with a relative afferent pupillary defect. Invest Ophthalmol Vis Sci. 2010; 51: 5049-5053.
42. Johnson LN, Hill RA, Bartholomew MJ. Correlation of afferent pupillary defect with visual field loss on automated perimetry. Ophthalmology. 1988; 95: 1649-1655.
43. Schiefer U, Dietzsch J, Dietz K, et al. Associating the magnitude of relative afferent pupillary defect (RAPD) with visual field indices in glaucoma patients. Br J Ophthalmol. 2012; 96: 629-633.
44. Tatsumi Y, Nakamura M, Fujioka M, et al. Quantification of retinal nerve fiber layer thickness reduction associated with a relative afferent pupillary defect in asymmetric glaucoma. Br J Ophthalmol. 2007; 91: 633-637.
45. 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.
46. Chang DS, Boland MV, Arora KS, Supakontanasan W, Chen BB, Friedman DS. Symmetry of the pupillary light reflex and its relationship to retinal nerve fiber layer thickness and visual field defect. Invest Ophthalmol Vis Sci. 2013; 54: 5596-5601.
47. von Bussmann KA, Garey LJ, Jen LS. Injury-resistant retinal ganglion cells that are rich in cytochrome oxidase. Neuroreport. 1993; 4: 247-250.
48. Lei S, Goltz HC, Chandrakumar M, Wong AM. Full-field chromatic pupillometry for the assessment of the postillumination pupil response driven by melanopsin-containing retinal ganglion cells. Invest Ophthalmol Vis Sci. 2014; 55: 4496-4503.
49. Kankipati L, Girkin CA, Gamlin PD. Post-illumination pupil response in subjects without ocular disease. Invest Ophthalmol Vis Sci. 2010; 51: 2764-2769.
50. Thordsen JE, Bower KS, Warren BB, Stutzman R. Miotic effect of brimonidine tartrate 0. 15% ophthalmic solution in normal eyes. J Cataract Refract Surg. 2004; 30: 1702-1706.
51. Brown SM, Khanani AM. Effect of brimonidine on pupil diameter. J Cataract Refract Surg. 2005; 31: 1686-1687.
52. McDonald JE II, El-Moatassem Kotb AM, Decker BB. Effect of brimonidine tartrate ophthalmic solution 0. 2% on pupil size in normal eyes under different luminance conditions. J Cataract Refract Surg. 2001; 27: 560-564.
53. Brown SM, Khanani AM, McCartney DL. The effect of daily use of brimonidine tartrate on the dark-adapted pupil diameter. Am J Ophthalmol. 2004; 138: 149-151.