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Efferent influences on the bioelectrical activity of the retina in primates

Documenta Ophthalmologica volume 134, pages 57–73 (2017)Cite this article

Abstract

Purpose

The existence of retinopetal (sometimes referred to as “efferent” or “centrifugal”) axons in the mammalian optic nerve is a topic of long-standing debate. Opposition is fading as efferent innervation of the retina has now been widely documented in rodents and other animals. The existence and function of an efferent system in humans and non-human primates has not, though, been definitively established. Such a feedback pathway could have important functional, clinical, and experimental significance to the field of vision science and ophthalmology.

Methods

Following a comprehensive literature review (PubMed and Google Scholar, until July 2016), we present evidence regarding a system that can influence the bioelectrical activity of the retina in primates.

Results

Anatomical and physiological evidences are presented separately. Improvements in histological staining and the advent of retrograde nerve fiber tracers have allowed for more confidence in the identification of efferent optic nerve fibers, including back to their point of origin.

Conclusion

Even with the accumulation of more modern anatomical and physiological evidence, some limitations and uncertainties about crucial details regarding the origins and role of a top–down, efferent system still exist. However, the summary of the evidence from earlier and more modern studies makes a compelling case in support of such a system in humans and non-human primates.

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References

  1. Miceli D, Reperant J, Bertrand C, Rio JP (1999) Functional anatomy of the avian centrifugal visual system. Behav Brain Res 98(2):203–210

    CAS  PubMed  Article  Google Scholar 

  2. Reperant J, Miceli D, Vesselkin NP, Molotchnikoff S (1989) The centrifugal visual system of vertebrates: a century-old search reviewed. Int Rev Cytol 118:115–171

    CAS  PubMed  Article  Google Scholar 

  3. Reperant J, Ward R, Miceli D, Rio JP, Medina M, Kenigfest NB, Vesselkin NP (2006) The centrifugal visual system of vertebrates: a comparative analysis of its functional anatomical organization. Brain Res Rev 52(1):1–57. doi:10.1016/j.brainresrev.2005.11.008

    CAS  PubMed  Article  Google Scholar 

  4. Avellaneda-Chevrier VK, Wang X, Hooper ML, Chauhan BC (2015) The retino-retinal projection: tracing retinal ganglion cells projecting to the contralateral retina. Neurosci Lett 591:105–109. doi:10.1016/j.neulet.2015.02.033

    CAS  PubMed  Article  Google Scholar 

  5. Nadal-Nicolas FM, Valiente-Soriano FJ, Salinas-Navarro M, Jimenez-Lopez M, Vidal-Sanz M, Agudo-Barriuso M (2015) Retino-retinal projection in juvenile and young adult rats and mice. Exp Eye Res 134:47–52. doi:10.1016/j.exer.2015.03.015

    CAS  PubMed  Article  Google Scholar 

  6. Tang X, Tzekov R, Passaglia CL (2016) Retinal cross talk in the mammalian visual system. J Neurophysiol 115(6):3018–3029. doi:10.1152/jn.01137.2015

    PubMed  Article  Google Scholar 

  7. Lansford TG, Baker HD (1969) Dark adaptation: an interocular light-adaptation effect. Science 164(3885):1307–1309

    CAS  PubMed  Article  Google Scholar 

  8. Makous W, Teller D, Boothe R (1976) Binocular interaction in the dark. Vis Res 16(5):473–476

    CAS  PubMed  Article  Google Scholar 

  9. Auerbach E, Peachey NS (1984) Interocular transfer and dark adaptation to long-wave test lights. Vis Res 24(9):1043–1048

    CAS  PubMed  Article  Google Scholar 

  10. Denny N, Frumkes TE, Barris MC, Eysteinsson T (1991) Tonic interocular suppression and binocular summation in human vision. J Physiol 437:449–460

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Eysteinsson T, Barris MC, Denny N, Frumkes TE (1993) Tonic interocular suppression, binocular summation, and the visual evoked potential. Invest Ophthalmol Vis Sci 34(8):2443–2448

    CAS  PubMed  Google Scholar 

  12. Freeman AW, Jolly N (1994) Visual loss during interocular suppression in normal and strabismic subjects. Vis Res 34(15):2043–2050

    CAS  PubMed  Article  Google Scholar 

  13. Huang PC, Baker DH, Hess RF (2012) Interocular suppression in normal and amblyopic vision: spatio-temporal properties. J Vis. doi:10.1167/12.11.29

    Google Scholar 

  14. Favreau OE (1978) Interocular transfer of color-contingent motion aftereffects: positive aftereffects. Vis Res 18(7):841–844

    CAS  PubMed  Article  Google Scholar 

  15. Wade NJ, Swanston MT, de Weert CM (1993) On interocular transfer of motion aftereffects. Perception 22(11):1365–1380

    CAS  PubMed  Article  Google Scholar 

  16. Nishida S, Ashida H (2000) A hierarchical structure of motion system revealed by interocular transfer of flicker motion aftereffects. Vis Res 40(3):265–278

    CAS  PubMed  Article  Google Scholar 

  17. Erkelens CJ, Van ER (1997) Capture of the visual direction of monocular objects by adjacent binocular objects. Vis Res 37(13):1735–1745

    CAS  PubMed  Article  Google Scholar 

  18. Raghunandan A (2011) Binocular capture: the effects of spatial frequency and contrast polarity of the monocular target. Vis Res 51(23–24):2369–2377. doi:10.1016/j.visres.2011.09.011

    PubMed  Article  Google Scholar 

  19. Kergoat H, Lovasik JV (1994) Unilateral ocular vascular stress in man and retinal responsivity in the contralateral eye. Ophthalmic Physiol Opt 14(4):401–407

    CAS  PubMed  Article  Google Scholar 

  20. Lovasik JV, Kergoat H, Gagnon M (2005) Experimentally reduced perfusion of one eye impairs retinal function in both eyes. Optom Vis Sci 82(9):850–857

    PubMed  Article  Google Scholar 

  21. Francis JH, Abramson DH, Marr BP, Brodie SE (2013) Ocular manipulation reduces both ipsilateral and contralateral electroretinograms. Doc Ophthalmol 127(2):113–122. doi:10.1007/s10633-013-9391-0

    PubMed  Article  Google Scholar 

  22. Polyak SL (1941) The retina. University of Chicago Press, Chicago

    Google Scholar 

  23. Honrubia FM, Elliott JH (1968) Efferent innervation of the retina. I. Morphologic study of the human retina. Arch Ophthalmol 80(1):98–103

    CAS  PubMed  Article  Google Scholar 

  24. Brooke RN, Downer Jde C, Powell TP (1965) Centrifugal fibres to the retina in the monkey and cat. Nature 207(5004):1365–1367

    CAS  PubMed  Article  Google Scholar 

  25. Noback CR, Mettler F (1973) Centrifugal fibers to the retina in the rhesus monkey. Brain Behav Evol 7(5):382–389

    CAS  PubMed  Article  Google Scholar 

  26. Itaya SK (1980) Retinal efferents from the pretectal area in the rat. Brain Res 201(2):436–441

    CAS  PubMed  Article  Google Scholar 

  27. Itaya SK, Itaya PW (1985) Centrifugal fibers to the rat retina from the medial pretectal area and the periaqueductal grey matter. Brain Res 326(2):362–365

    CAS  PubMed  Article  Google Scholar 

  28. Labandeira-Garcia JL, Guerra-Seijas MJ, Gonzalez F, Perez R, Acuna C (1990) Location of neurons projecting to the retina in mammals. Neurosci Res 8(4):291–302

    CAS  PubMed  Article  Google Scholar 

  29. Frazao R, Pinato L, da Silva AV, Britto LR, Oliveira JA, Nogueira MI (2008) Evidence of reciprocal connections between the dorsal raphe nucleus and the retina in the monkey Cebus apella. Neurosci Lett 430(2):119–123. doi:10.1016/j.neulet.2007.10.032

    CAS  PubMed  Article  Google Scholar 

  30. Abudureheman A, Nakagawa S (2010) Retinopetal neurons located in the diencephalon of the Japanese monkey (Macaca fuscata). Okajimas Folia Anat Jpn 87(1):17–23

    PubMed  Article  Google Scholar 

  31. Gastinger MJ, O’Brien JJ, Larsen NB, Marshak DW (1999) Histamine immunoreactive axons in the macaque retina. Invest Ophthalmol Vis Sci 40(2):487–495

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Gastinger MJ, Bordt AS, Bernal MP, Marshak DW (2005) Serotonergic retinopetal axons in the monkey retina. Curr Eye Res 30(12):1089–1095. doi:10.1080/02713680500371532

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Yu YC, Satoh H, Wu SM, Marshak DW (2009) Histamine enhances voltage-gated potassium currents of ON bipolar cells in macaque retina. Invest Ophthalmol Vis Sci 50(2):959–965. doi:10.1167/iovs.08-2746

    PubMed  Article  Google Scholar 

  34. Vila A, Satoh H, Rangel C, Mills SL, Hoshi H, O’Brien J, Marshak DR, Macleish PR, Marshak DW (2012) Histamine receptors of cones and horizontal cells in old world monkey retinas. J Comp Neurol 520(3):528–543. doi:10.1002/cne.22731

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Sharif NA, Senchyna M (2006) Serotonin receptor subtype mRNA expression in human ocular tissues, determined by RT-PCR. Mol Vis 12:1040–1047

    CAS  PubMed  Google Scholar 

  36. Dowling JE, Boycott BB (1966) Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166(1002):80–111

    CAS  PubMed  Article  Google Scholar 

  37. Dowling JE, Boycott BB (1969) Retinal ganglion cells: a correlation of anatomical and physiological approaches. UCLA Forum Med Sci 8:145–161

    CAS  PubMed  Google Scholar 

  38. Honrubia FM, Elliott JH (1970) Efferent innervation of the retina. II. Morphologic study of the monkey retina. Invest Ophthalmol 9(12):971–976

    CAS  PubMed  Google Scholar 

  39. Anderson DR (1973) Ascending and descending optic atrophy produced experimentally in squirrel monkeys. Am J Ophthalmol 76(5):693–711

    CAS  PubMed  Article  Google Scholar 

  40. Khosla PK, Saini JS, Gahlot DK, Ratnakar KS (1981) Effect of optic nerve sectioning on e.r.g. (a electrophysiological and histological experimental study). Indian J Ophthalmol 29(3):263–267

    CAS  PubMed  Google Scholar 

  41. Silveira LC, Perry VH (1990) A neurofibrillar staining method for retina and skin: a simple modification for improved staining and reliability. J Neurosci Methods 33(1):11–21

    CAS  PubMed  Article  Google Scholar 

  42. Usai C, Ratto GM, Bisti S (1991) Two systems of branching axons in monkey’s retina. J Comp Neurol 308(2):149–161. doi:10.1002/cne.903080202

    CAS  PubMed  Article  Google Scholar 

  43. Perry VH, Oehler R, Cowey A (1984) Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12(4):1101–1123

    CAS  PubMed  Article  Google Scholar 

  44. Polyak SL (1957) The vertebrate visual system; its origin, structure, and function and its manifestations in disease with an analysis of its role in the life of animals and in the origin of man, preceded by a historical review of investigations of the eye, and of the visual pathways and centers of the brain. University of Chicago Press, Chicago

  45. Warrington WB, Dutton JE (1900) Observations of the course of the optic fibers in a case of unilateral optic atrophy. Brain 23(4):642–656

    Article  Google Scholar 

  46. Liss L, Wolter JR (1956) Centrifugal (antidromic) nerve fibers in the optic nerve of man. Albrecht Von Graefes Arch Ophthalmol 158(1):1–7

    CAS  PubMed  Article  Google Scholar 

  47. Knöferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, Tönges L, Stadelmann C, Brück W, Bähr M, Lingor P (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci 107(13):6064–6069. doi:10.1073/pnas.0909794107

    PubMed  PubMed Central  Article  Google Scholar 

  48. Vanburen JM (1963) Trans-synaptic retrograde degeneration in the visual system of primates. J Neurol Neurosurg Psychiatry 26:402–409

    CAS  PubMed  Article  Google Scholar 

  49. Wolter JR (1965) The centrifugal nerves in the human optic tract, chiasm, optic nerve, and retina. Trans Am Ophthalmol Soc 63:678–707

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Ventura J, Mathieu M (1960) Silver impregnation of whole retinas. Arch Ophthalmol 64:528–535

    CAS  PubMed  Article  Google Scholar 

  51. Wolter JR (1957) Ending of centrifugal nerve fibers on the blood vessels of the human retina. Albrecht Von Graefes Arch Ophthalmol 158(6):524–531

    CAS  PubMed  Article  Google Scholar 

  52. Wolter JR (1961) Diabetic retinopathy. Am J Ophthalmol 51:1123–1141

    CAS  PubMed  Google Scholar 

  53. Pfister RR, Wolter JR (1963) Centrifugal fibers of the human optic nerve. A study made five days after enucleation. Neurology 13:38–42

    CAS  PubMed  Article  Google Scholar 

  54. Wolter JR, Knoblich RR (1965) Pathway of centrifugal fibres in the human optic nerve, chiasm, and tract. Br J Ophthalmol 49:246–250

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. Wolter JR, Moorman LT (1966) Early effects of photocoagulation on the nerve fiber layer of the human retina. Arch Ophthalmol 76(3):385–390

    CAS  PubMed  Article  Google Scholar 

  56. Wolter JR, Lund OE (1968) Reaction of centrifugal nerves in the human retina two weeks after photocoagulation. Trans Am Ophthalmol Soc 66:173–195

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. Sacks JG, Lindenberg R (1969) Efferent nerve fibers in the anterior visual pathways in bilateral congenital cystic eyeballs. Am J Ophthalmol 68(4):691–695

    CAS  PubMed  Article  Google Scholar 

  58. Reperant J, Gallego A (1976) Centrifugal fibers in the human retina. Arch Anat Microsc Morphol Exp 65(2):103–120

    CAS  PubMed  Google Scholar 

  59. Wolter JR (1979) Electron microscopic demonstration of centrifugal nerve fibers in the human optic nerve. Albrecht Von Graefes Arch Klin Exp Ophthalmol 210(1):31–41

    CAS  PubMed  Article  Google Scholar 

  60. Wolter JR (1991) Reaction of centrifugal nerves in perforated peripheral retina. Neuro-Ophthalmology 11(4):189–193. doi:10.3109/01658109109036955

    Article  Google Scholar 

  61. Thanos S (1999) Genesis, neurotrophin responsiveness, and apoptosis of a pronounced direct connection between the two eyes of the chick embryo: a natural error or a meaningful developmental event? J Neurosci 19(10):3900–3917

    CAS  PubMed  Google Scholar 

  62. Bunt SM, Lund RD (1981) Development of a transient retino-retinal pathway in hooded and albino rats. Brain Res 211(2):399–404

    CAS  PubMed  Article  Google Scholar 

  63. Muller M, Hollander H (1988) A small population of retinal ganglion cells projecting to the retina of the other eye. An experimental study in the rat and the rabbit. Exp Brain Res 71(3):611–617

    CAS  PubMed  Article  Google Scholar 

  64. Dean G, Usher CH (1896) Experimental research on the course of the optic fibers. Trans Ophthalmol Soc UK 16:248–276

    Google Scholar 

  65. Dean G, Usher CH (1903) Experimental research on the cours4e of the optic fibers. Brian 26:524–546

    Article  Google Scholar 

  66. Parsons J (1902) Degenerations following lesions of the retin in monkeys. Brain 25:257–269

    Article  Google Scholar 

  67. Pick A, Herrenheiser J (1895) Untersuchungen über die topographischen Beziehungen zwischen Retina, Opticus und gekreuztem Tractus opticus beim Kaninchen. Nova Acta der Kaiserl Leop Carol Deutchen Acad der Naturf 66(1):1–24

    Google Scholar 

  68. Meyer A (1904) The anatomical facts and clinical varieties of traumatic insanity. Am J Insanity 60(3):373–441

    Google Scholar 

  69. Molotchnikoff S, Lachapelle P, Casanova C (1989) Optic nerve blockade influences the retinal responses to flash in rabbits. Vis Res 29(8):957–963

    CAS  PubMed  Article  Google Scholar 

  70. Borg E, Knave B (1971) Long-term changes in the ERG following transection of the optic nerve in the rabbit. Acta Physiol Scand 82(2):277–281. doi:10.1111/j.1748-1716.1971.tb04968.x

    CAS  PubMed  Article  Google Scholar 

  71. Jacobson JH, Suzuki TA (1962) Effects of optic nerve section on the ERG. Arch Ophthalmol 67:791–801

    CAS  PubMed  Article  Google Scholar 

  72. Galambos R, Juhasz G, Kekesi AK, Nyitrai G, Szilagyi N (1994) Natural sleep modifies the rat electroretinogram. Proc Natl Acad Sci USA 91(11):5153–5157

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Molotchnikoff S, Tremblay F (1983) Influence of the visual cortex on responses of retinal ganglion cells in the rat. J Neurosci Res 10(4):397–409. doi:10.1002/jnr.490100407

    CAS  PubMed  Article  Google Scholar 

  74. Jacobson JH, Gestring GF (1958) Centrifugal influence upon the electroretinogram. AMA Arch Ophthalmol 60(2):295–302

    CAS  PubMed  Article  Google Scholar 

  75. Haft JS, Harman PJ (1967) Evidence for central inhibition of retinal function. Vision Res 7(5):499–501

    CAS  PubMed  Article  Google Scholar 

  76. Haft JS (1968) Further remarks on evidence for central inhibition of retinal function. Vis Res 8(3):319–323

    CAS  PubMed  Article  Google Scholar 

  77. Abe N (1962) Effect of section and compression of the optic nerve on the ERG in the rabbit. Tohoku J Exp Med 78:223–227

    CAS  PubMed  Article  Google Scholar 

  78. Mirsky AF, Bloch S, Tecce JJ, Lessell S, Marcus E (1973) Visual evoked potentials during experimentally induced spike-wave activity in monkeys. Electroencephalogr Clin Neurophysiol 35(1):25–37

    CAS  PubMed  Article  Google Scholar 

  79. Maffei L, Fiorentini A, Bisti S, Hollander H (1985) Pattern ERG in the monkey after section of the optic nerve. Exp Brain Res 59(2):423–425

    CAS  PubMed  Article  Google Scholar 

  80. Maertz NA, Kim CB, Nork TM, Levin LA, Lucarelli MJ, Kaufman PL, Ver Hoeve JN (2006) Multifocal visual evoked potentials in the anesthetized non-human primate. Curr Eye Res 31(10):885–893. doi:10.1080/02713680600899648

    PubMed  Article  Google Scholar 

  81. Ogden TE, Brown KT (1964) Intraretinal responses of the cynamolgus monkey to electrical stimulation of the optic nerve and retina. J Neurophysiol 27:682–705

    CAS  PubMed  Google Scholar 

  82. Ogden TE (1966) Intraretinal slow potentials evoked by brain stimulation in the primate. J Neurophysiol 29(5):898–908

    CAS  PubMed  Google Scholar 

  83. Gouras P (1969) Antidromic responses of orthodromically identified ganglion cells in monkey retina. J Physiol 204(2):407–419

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Ogden TE (1973) The oscillatory waves of the primate electroretinogram. Vis Res 13(6):1059–1074

    CAS  PubMed  Article  Google Scholar 

  85. Ogden TE (1973) The proximal negative response of the primate retina. Vis Res 13(4):797–807

    CAS  PubMed  Article  Google Scholar 

  86. Fukuda Y, Watanabe M, Wakakuwa K, Sawai H, Morigiwa K (1988) Intraretinal axons of ganglion cells in the Japanese monkey (Macaca fuscata): conduction velocity and diameter distribution. Neurosci Res 6(1):53–71

    CAS  PubMed  Article  Google Scholar 

  87. Fukuda Y, Sawai H, Watanabe M, Wakakuwa K, Morigiwa K (1989) Nasotemporal overlap of crossed and uncrossed retinal ganglion cell projections in the Japanese monkey (Macaca fuscata). J Neurosci 9(7):2353–2373

    CAS  PubMed  Google Scholar 

  88. Raviola E, Raviola G (1982) Structure of the synaptic membranes in the inner plexiform layer of the retina: a freeze-fracture study in monkeys and rabbits. J Comp Neurol 209(3):233–248. doi:10.1002/cne.902090303

    CAS  PubMed  Article  Google Scholar 

  89. Kenyon GT, Travis BJ, Theiler J, George JS, Stephens GJ, Marshak DW (2004) Stimulus-specific oscillations in a retinal model. IEEE Trans Neural Netw 15(5):1083–1091. doi:10.1109/TNN.2004.832722

    PubMed  Article  Google Scholar 

  90. Hood DC, Frishman LJ, Saszik S, Viswanathan S (2002) Retinal origins of the primate multifocal ERG: implications for the human response. Invest Ophthalmol Vis Sci 43(5):1673–1685

    PubMed  Google Scholar 

  91. Gastinger MJ, Barber AJ, Vardi N, Marshak DW (2006) Histamine receptors in mammalian retinas. J Comp Neurol 495(6):658–667. doi:10.1002/cne.20902

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  92. Nork TM, Kim CB, Heatley GA, Kaufman PL, Lucarelli MJ, Levin LA, Ver Hoeve JN (2010) Serial multifocal electroretinograms during long-term elevation and reduction of intraocular pressure in non-human primates. Doc Ophthalmol 120(3):273–289. doi:10.1007/s10633-010-9231-4

    PubMed  PubMed Central  Article  Google Scholar 

  93. Nork TM, Kim CB, Munsey KM, Dashek RJ, Hoeve JN (2014) Regional choroidal blood flow and multifocal electroretinography in experimental glaucoma in rhesus macaques. Invest Ophthalmol Vis Sci 55(12):7786–7798. doi:10.1167/iovs.14-14527

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. Hood DC, Frishman LJ, Viswanathan S, Robson JG, Ahmed J (1999) Evidence for a ganglion cell contribution to the primate electroretinogram (ERG): effects of TTX on the multifocal ERG in macaque. Vis Neurosci 16(3):411–416

    CAS  PubMed  Article  Google Scholar 

  95. Hare WA, Ton H (2002) Effects of APB, PDA, and TTX on ERG responses recorded using both multifocal and conventional methods in monkey. Effects of APB, PDA, and TTX on monkey ERG responses. Doc Ophthalmol 105(2):189–222

    PubMed  Article  Google Scholar 

  96. Hare WA, WoldeMussie E, Lai RK, Ton H, Ruiz G, Chun T, Wheeler L (2004) Efficacy and safety of memantine treatment for reduction of changes associated with experimental glaucoma in monkey, I: functional measures. Invest Ophthalmol Vis Sci 45(8):2625–2639. doi:10.1167/iovs.03-0566

    PubMed  Article  Google Scholar 

  97. Sutter EE, Bearse MA Jr (1999) The optic nerve head component of the human ERG. Vis Res 39(3):419–436

    CAS  PubMed  Article  Google Scholar 

  98. Hood DC, Bearse MA Jr, Sutter EE, Viswanathan S, Frishman LJ (2001) The optic nerve head component of the monkey’s (Macaca mulatta) multifocal electroretinogram (mERG). Vis Res 41(16):2029–2041

    CAS  PubMed  Article  Google Scholar 

  99. Perry VH, Cowey A (1985) The ganglion cell and cone distributions in the monkey’s retina: implications for central magnification factors. Vis Res 25(12):1795–1810

    CAS  PubMed  Article  Google Scholar 

  100. Curcio CA, Allen KA (1990) Topography of ganglion cells in human retina. J Comp Neurol 300(1):5–25. doi:10.1002/cne.903000103

    CAS  PubMed  Article  Google Scholar 

  101. Jonas JB, Schneider U, Naumann GO (1992) Count and density of human retinal photoreceptors. Graefes Arch Clin Exp Ophthalmol 230(6):505–510

    CAS  PubMed  Article  Google Scholar 

  102. Silveira LC, Perry VH (1991) The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina. Neuroscience 40(1):217–237

    CAS  PubMed  Article  Google Scholar 

  103. Silveira LC, Perry VH, Yamada ES (1993) The retinal ganglion cell distribution and the representation of the visual field in area 17 of the owl monkey, Aotus trivirgatus. Vis Neurosci 10(5):887–897

    CAS  PubMed  Article  Google Scholar 

  104. Silva MF, Maia-Lopes S, Mateus C, Guerreiro M, Sampaio J, Faria P, Castelo-Branco M (2008) Retinal and cortical patterns of spatial anisotropy in contrast sensitivity tasks. Vis Res 48(1):127–135. doi:10.1016/j.visres.2007.10.018

    PubMed  Article  Google Scholar 

  105. Silva MF, Mateus C, Reis A, Nunes S, Fonseca P, Castelo-Branco M (2010) Asymmetry of visual sensory mechanisms: electrophysiological, structural, and psychophysical evidences. J Vis 10(6):26. doi:10.1167/10.6.26

    PubMed  Article  Google Scholar 

  106. Wirth A (1951) Note on the mechanism of inter-retinal reflexes. Boll Ocul 30(8):499–504

    CAS  PubMed  Google Scholar 

  107. Dodt E (1951) On the electrophysiology of the eye. I. Secondary elevation of the electroretinogram in response to illumination. Albrecht Von Graefes Arch Ophthalmol 151(7–8):672–692

    CAS  PubMed  Article  Google Scholar 

  108. Motokawa K, Nakagawa D, Kohata T (1956) Electrophysiological studies of binocular stereoscopic vision. J Comp Physiol Psychol 49(4):398–403

    CAS  PubMed  Article  Google Scholar 

  109. Steindler P, Cardin P, Perrone S (1981) The electric consensual response of the non-stimulated eye in normal subjects and patients with optic atrophy. Albrecht Von Graefes Arch Klin Exp Ophthalmol 216(2):121–127

    CAS  PubMed  Article  Google Scholar 

  110. Uchermann A (1955) The electroretinogram on binocular and monocular light stimulation. Acta Ophthalmol (Copenh) 33(5):517–522

    CAS  Article  Google Scholar 

  111. Bagolini B (1959) The electroretinogram during monocular and binocular stimulations. Boll Ocul 38:605–615

    CAS  PubMed  Google Scholar 

  112. Monnier M (1946) Les manifestations electriques consensuelles de l’activite retinienne chez l’homme (electroretinographie binoculaire). Experientia 2:190

    CAS  PubMed  Article  Google Scholar 

  113. Monnier M (1949) L’electro-retinogramme de l’homme. Electroencephalogr Clin Neurophysiol 1(1):87–108

    CAS  PubMed  Article  Google Scholar 

  114. Marg E (1953) The effect of stimulus size and retinal illuminance on the human electroretinogram. Am J Optom Arch Am Acad Optom 30(8):417–433

    CAS  PubMed  Article  Google Scholar 

  115. Hellner KA (1964) Efferent inhibition of single erg-responses by flicker-stimulation of the contralateral eye in man. Doc Ophthalmol 18:431–439

    CAS  PubMed  Article  Google Scholar 

  116. Nikitopoulou-Maratou G, Vassiliou GA, Kepetzis M, Molyvdas PA (1980) ERG alterations induced by sound. Neurochem Int 1C:355–365

    CAS  PubMed  Article  Google Scholar 

  117. Hernandez-Peon R, Scherrer H, Jouvet M (1956) Modification of electric activity in cochlear nucleus during attention in unanesthetized cats. Science 123(3191):331–332

    CAS  PubMed  Article  Google Scholar 

  118. Lindsley DB (1960) Attention, consciousness, sleep and wakefulness. In: Field J, Magoun HW, Hall VA (eds) Handbook of physiology. American Physiological Society, Washington, DC, pp 1553–1593

    Google Scholar 

  119. Spinelli DN, Weingarten M (1966) Afferent and efferent activity in single units of the cat’s optic nerve. Exp Neurol 15(3):347–362

    CAS  PubMed  Article  Google Scholar 

  120. Van Hasselt P (1972) The centrifugal control of retinal function. Ophthalmic Res 4(5):298–320

    Article  Google Scholar 

  121. Luck SJ, Woodman GF, Vogel EK (2000) Event-related potential studies of attention. Trends Cogn Sci 4(11):432–440

    CAS  PubMed  Article  Google Scholar 

  122. Naatanen R (1975) Selective attention and evoked potentials in humans–a critical review. Biol Psychol 2(4):237–307

    CAS  PubMed  Article  Google Scholar 

  123. Eason RG (1984) Selective attention effects on retinal and forebrain responses in humans: a replication and extension. Bull Psychon Soc 22(4):341–344. doi:10.3758/bf03333837

    Article  Google Scholar 

  124. Wasserman GS, Bolbecker AR, Li J, Lim-Kessler CC (2010) No retinal efference in humans: an urban legend. Proc Fechner Day 26(1):257–262

    Google Scholar 

  125. Wasserman GS, Bolbecker AR, Li J, Lim-Kessler CC (2011) A top-down and bottom-up component of visual attention. Cognitive Comput 3(1):294–302

    Article  Google Scholar 

  126. Kahneman D, Beatty J (1966) Pupil diameter and load on memory. Science 154(3756):1583–1585

    CAS  PubMed  Article  Google Scholar 

  127. Mathot S, Van der Stigchel S (2015) New light on the mind’s eye: the pupillary light response as active vision. Curr Dir Psychol Sci 24(5):374–378. doi:10.1177/0963721415593725

    PubMed  PubMed Central  Article  Google Scholar 

  128. Anthony BJ, Graham FK (1985) Blink reflex modification by selective attention: evidence for the modulation of ‘automatic’ processing. Biol Psychol 21(1):43–59

    CAS  PubMed  Article  Google Scholar 

  129. Hackley SA, Woldorff M, Hillyard SA (1990) Cross-modal selective attention effects on retinal, myogenic, brainstem, and cerebral evoked potentials. Psychophysiology 27(2):195–208

    CAS  PubMed  Article  Google Scholar 

  130. Eason RG, Flowers L, Oakley M (1983) Differentiation of retinal and nonretinal contributions to averaged evoked responses obtained with electrodes placed near the eyes. Behav Res Methods Instrum 15(1):13–21. doi:10.3758/bf03203432

    Article  Google Scholar 

  131. Eason RG, Oakley M, Flowers L (1983) Central neural influences on the human retina during selective attention. Physiol Psychol 11(1):18–28. doi:10.3758/bf03326765

    Article  Google Scholar 

  132. Mangun GR, Hansen JC, Hillyard SA (1986) Electroretinograms reveal no evidence for centrifugal modulation of retinal inputs during selective attention in man. Psychophysiology 23(2):156–165

    CAS  PubMed  Article  Google Scholar 

  133. Karpe G (1945) The basis of clinical electroretinography. Acta Ophthalmol Suppl 24:1–118

    Google Scholar 

  134. Dieterle P, Babel J (1955) Diagnostic importance of simultaneous registration of the electroretinogram and the electroencephalogram (retinocortical time measurement) in optic tract diseases. Ophthalmologica 129(4–5):245–247

    CAS  PubMed  Article  Google Scholar 

  135. Suzuki TA (1959) ERG of congenital totally color-weak eye accompanied by lesion of optic nerve. Arch Ophthalmol 62:386–395

    CAS  PubMed  Article  Google Scholar 

  136. Gills JP Jr (1966) The electroretinogram after section of the optic nerve in man. Am J Ophthalmol 62(2):287–291

    PubMed  Article  Google Scholar 

  137. Feinsod M, Auerbach E (1973) Electrophysiological examinations of the visual system in the acute phase after head injury. Eur Neurol 9(1):56–64

    CAS  PubMed  Article  Google Scholar 

  138. Hillman JS, Myska V, Nissim S (1975) Complete avulsion of the optic nerve. A clinical, angiographic, and electrodiagnostic study. Br J Ophthalmol 59(9):503–509

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  139. Müller W, Schmöger E (1981) Postoperative electrophysiological findings in patients with pituitary adenoma. In: Spekreijse H, Apkarian PA (eds) Visual pathways: electrophysiology and pathology. Springer, Dordrecht, pp 203–211. doi:10.1007/978-94-009-8656-5_21

    Chapter  Google Scholar 

  140. Dawson WW, Maida TM, Rubin ML (1982) Human pattern-evoked retinal responses are altered by optic atrophy. Invest Ophthalmol Vis Sci 22(6):796–803

    CAS  PubMed  Google Scholar 

  141. Feinsod M, Rowe H, Auerbach E (1971) Changes in the electroretinogram in patients with optic nerve lesions. Doc Ophthalmol 29(2):169–200

    CAS  PubMed  Article  Google Scholar 

  142. Feinsod M, Auerbach E (1971) The electroretinogram and the visual evoked potential in two patients with tuberculum sellae meningioma before and after decompression of the optic nerve. Ophthalmologica 163(5):360–368

    CAS  PubMed  Article  Google Scholar 

  143. Ikeda H, Tremain KE, Sanders MD (1978) Neurophysiological investigation in optic nerve disease: combined assessment of the visual evoked response and electroretinogram. Br J Ophthalmol 62(4):227–239

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  144. Kaitz M, Perlman I, Ovadia N, Ankava D, Auerbach E, Feinsod M (1982) Visual defects in the uninjured eye of patients with unilateral eye injury. Doc Ophthalmol 53(2):179–190

    CAS  PubMed  Article  Google Scholar 

  145. Wachtmeister L, El Azazi M (1985) Oscillatory potentials of the electroretinogram in patients with unilateral optic atrophy. Ophthalmologica 191(1):39–50

    CAS  PubMed  Article  Google Scholar 

  146. Vaegan Graham SL, Goldberg I, Buckland L, Hollows FC (1995) Flash and pattern electroretinogram changes with optic atrophy and glaucoma. Exp Eye Res 60(6):697–706

    CAS  PubMed  Article  Google Scholar 

  147. Fraser CL, Holder GE (2011) Electroretinogram findings in unilateral optic neuritis. Doc Ophthalmol 123(3):173–178. doi:10.1007/s10633-011-9294-x

    PubMed  Article  Google Scholar 

  148. Smith KJ, McDonald WI (1999) The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease. Philos Trans R Soc Lond B Biol Sci 354(1390):1649–1673. doi:10.1098/rstb.1999.0510

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  149. Pittock SJ, Lucchinetti CF (2007) The pathology of MS: new insights and potential clinical applications. Neurologist 13(2):45–56. doi:10.1097/01.nrl.0000253065.31662.37

    PubMed  Article  Google Scholar 

  150. Landois L (1904) The cranial nerves. In: Brubaker AP (ed) Textbook of human physiology, including histology and human anatomy, 10th edn. Blakiston's Son & Co., Philadelphia, p 529

  151. Landois L (1904) The visual apparatus. In: Brubaker AP (ed) Textbook of human physiology, including histology and microscopic anatomy. P. Blakiston’s, Philadelphia, p 819

    Google Scholar 

  152. Tigerstedt R (1910) Vision. In: Murlin JR (ed) A textbook of human physiology. Appleton, New York, p 515

    Google Scholar 

  153. Bronson-Castain K, Bearse MA, Han Y, Schneck ME, Adams AJ (2005) An order effect in sequential testing using the multifocal electroretinogram (mfERG). Invest Ophthalmol Vis Sci 46(13):3437

    Google Scholar 

  154. Simonsen SE (1966) ERG in diabet. In: Paper presented at the clinical value of electroretinography. Symposium held in connection with the 20th International Congress of Ophthalmology Munich, August

  155. Gastinger MJ, Barber AJ, Khin SA, McRill CS, Gardner TW, Marshak DW (2001) Abnormal centrifugal axons in streptozotocin-diabetic rat retinas. Invest Ophthalmol Vis Sci 42(11):2679–2685

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Bodeutsch N, Siebert H, Dermon C, Thanos S (1999) Unilateral injury to the adult rat optic nerve causes multiple cellular responses in the contralateral site. J Neurobiol 38(1):116–128

    CAS  PubMed  Article  Google Scholar 

  157. Panagis L, Thanos S, Fischer D, Dermon CR (2005) Unilateral optic nerve crush induces bilateral retinal glial cell proliferation. Eur J Neurosci 21(8):2305–2309. doi:10.1111/j.1460-9568.2005.04046.x

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We are thankful to Geoffrey Arden, David Marshak, and William Hare for their comments on the text. We thank Alessandro Iannaccone for help with references written in Italian language.

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Authors and Affiliations

  1. Department of Ophthalmology, University of South Florida, 12901 Bruce B. Downs Blvd., MDC 21, Tampa, FL, 33612, USA

    Gonzalo Ortiz, Christopher L. Passaglia & Radouil T. Tzekov

  2. Department of Ophthalmology, West Virginia University, Morgantown, WV, USA

    J. Vernon Odom

  3. Department of Chemical and Biomedical Engineering, University of South Florida, Tampa, FL, USA

    Christopher L. Passaglia

  4. The Roskamp Institute, Sarasota, FL, USA

    Radouil T. Tzekov

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  1. Gonzalo Ortiz
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Correspondence to Radouil T. Tzekov.

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Ortiz, G., Odom, J.V., Passaglia, C.L. et al. Efferent influences on the bioelectrical activity of the retina in primates. Doc Ophthalmol 134, 57–73 (2017). https://doi.org/10.1007/s10633-016-9567-5

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Keywords

  • Centrifugal fibers
  • Efferent fibers
  • Retinopetal fibers
  • Retina
  • Electroretinogram