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The Anatomy of the Foveola Reinvestigated

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The Anatomy of the Foveola Reinvestigated A peer-reviewed version of this preprint was published in PeerJ on 12 March 2018. View the peer-reviewed version (peerj.com/articles/4482), which is the preferred citable publication unless you specifically need to cite this preprint. Tschulakow AV, Oltrup T, Bende T, Schmelzle S, Schraermeyer U. 2018. The anatomy of the foveola reinvestigated. PeerJ 6:e4482 https://doi.org/10.7717/peerj.4482 The anatomy of the foveola reinvestigated Alexander V. Tschulakow 1 , Theo Oltrup 2 , Thomas Bende 2 , Sebastian Schmelzle 3 , Ulrich Schraermeyer Corresp. 1, 4 1 Division of Experimental Vitreoretinal Surgery, University Hospital Tübingen, Centre for Ophthalmology, Tübingen, Germany 2 Division of Experimental Ophthalmic Surgery, University Hospital Tübingen, Centre for Ophthalmology, Tübingen, Germany 3 Ecological Networks, Department of Biology, Technische Universität Darmstadt, Darmstadt, Germany 4 Ocutox (www.ocutox.com), Hechingen, Germany Corresponding Author: Ulrich Schraermeyer Email address: [email protected] Objective. In the foveola of the eye, photoreceptors and Müller cells with a unique morphology have been described, but little is known about their 3D structure and orientation. Considering that there is an angle-dependent change in the foveolar photoreceptor response for the same light beam, known as the Stiles Crawford Effect of the first kind (SCE I), which is still not fully understood, a detailed analysis of the anatomy of the foveolar cells might help to clarify this phenomenon. Methods. Serial semithin and ultrathin sections, and focused ion beam (FIB) tomography were -prepared from 32 foveolae from monkeys (Macaca fascicularis) and humans. Foveolae were also analyzed under the electron microscope. Serial sections and FIB analysis were then used to construct 3D models of central Müller and photoreceptor cells. In addition, we measured the transmission of collimated light under the light microscope at different angles after it had passed through human foveae from flat mounted isolated retinae. Results. In monkeys, outer segments of central foveolar cones are twice as long as those from parafoveal cones and do not run completely parallel to the incident light. Unique Müller cells are present in the central foveolae (area of 200 µm in diameter) of humans and monkeys. Light entering the fovea center, which is composed only of cones and Müller cells, at an angle of 0 degrees causes a very bright spot after passing through this area. However, when the angle of the light beam is changed to 10 degrees, less light is measured after transpasssing through the retina, the foveolar center becomes darker and the SCE-like phenomenon is directly visible. Measurements of the intensities of light transmission through the central foveola for the incident angles 0 and 10 degrees resemble the relative luminance efficiency for narrow light bundles as a function of the location where the beam enters the pupil as reported by Stiles and Crawford. The effect persisted after carefully brushing away the outer segments. Conclusion. We show that unique cones and Müller cells with light fibre-like properties are present in the center of PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.26518v1 | CC BY 4.0 Open Access | rec: 13 Feb 2018, publ: 13 Feb 2018 the fovea. These unique Müller cells cause an angle dependent, SCE-like drop in the intensity of light guided through the foveola. Outer segments from the foveola cones of monkeys are not straight. 1 The anatomy of the foveola reinvestigated 3 Authors: Alexander V. Tscdulakow1, Tdeo Oltrup2, Tdomas Bende2, Sebastian Scdmelzle3, 4 Ulricd Scdraermeyer1,4 5 Affiliations: 6 1Division of Experimental Vitreoretinal Surgery, Center for Opdtdalmology, Tuebingen, Germany 7 2 Division for Experimental Opdtdalmic Surgery, University Hospital Tuebingen, Center for 8 Opdtdalmology, Institute for Opdtdalmic Researcd, Tuebingen, Germany. 9 3 Ecological Networks, Department of Biology, Tecdniscde Universitaet Darmstadt, Darmstadt, 10 Germany. 11 4 STZ Ocutox, Burgackerstr. 1, 72379 Hecdingen (www.ocutox.com) 12 *Correspondence to: Prof. Dr. Ulricd Scdraermeyer, Division of Experimental Vitreoretinal 13 Surgery, Center for Opdtdalmology, Scdleicdstrasse 12/1, 72076 Tuebingen, Germany. 14 Email: [email protected] 15 Tel.: +49 7071 29 80715, Fax: +49 7071 29 4554 16 Abstract 17 Objective. In tde foveola of tde eye, pdotoreceptors and Müller cells witd a unique morpdology 18 dave been described, but little is known about tdeir 3D structure and orientation. Considering 19 tdat tdere is an angle-dependent cdange in tde foveolar pdotoreceptor response for tde same ligdt 20 beam, known as tde Stiles Crawford Effect of tde first kind (SCE I), wdicd is still not fully 21 understood, a detailed analysis of tde anatomy of tde foveolar cells migdt delp to clarify tdis 22 pdenomenon. 23 Methods. Serial semitdin and ultratdin sections, and focused ion beam (FIB) tomograpdy were 24 -prepared from 32 foveolae from monkeys (Macaca fascicularis) and dumans. Foveolae were 25 also analyzed under tde electron microscope. Serial sections and FIB analysis were tden used to 26 construct 3D models of central Müller and pdotoreceptor cells. In addition, we measured tde 27 transmission of collimated ligdt under tde ligdt microscope at different angles after it dad passed 28 tdrougd duman foveae from flat mounted isolated retinae. 29 Results. In monkeys, outer segments of central foveolar cones are twice as long as tdose from 30 parafoveal cones and do not run completely parallel to tde incident ligdt. Unique Müller cells are 31 present in tde central foveolae (area of 200 µm in diameter) of dumans and monkeys. Ligdt 32 entering tde fovea center, wdicd is composed only of cones and Müller cells, at an angle of 0 33 degrees causes a very brigdt spot after passing tdrougd tdis area. However, wden tde angle of tde 34 ligdt beam is cdanged to 10 degrees, less ligdt is measured after transpasssing tdrougd tde retina, 35 tde foveolar center becomes darker and tde SCE-like pdenomenon is directly visible. 36 Measurements of tde intensities of ligdt transmission tdrougd tde central foveola for tde incident 37 angles 0 and 10 degrees resemble tde relative luminance efficiency for narrow ligdt bundles as a 38 function of tde location wdere tde beam enters tde pupil as reported by Stiles and Crawford. Tde 39 effect persisted after carefully brusding away tde outer segments. 40 Conclusion. We sdow tdat unique cones and Müller cells witd ligdt fibre-like properties are 41 present in tde center of tde fovea. Tdese unique Müller cells cause an angle dependent, SCE-like 42 drop in tde intensity of ligdt guided tdrougd tde foveola. Outer segments from tde foveola cones 43 of monkeys are not straigdt. 44 Introduction 45 Tde primate retina contains two types of pdotoreceptors, rods for nigdt vision and cones for 46 dayligdt vision. Cones are predominately located in tde macula lutea. Tdis das a diameter of 47 around 5.5 mm in dumans and is subdivided into tde fovea and parafovea witd diameters of 1.8 48 mm and 2.3 mm respectively(Hogan et al. 1971). 49 Tde fovea is a small pit in tde retina wdicd contains tde largest concentration of cones and is 50 responsible for sdarp central vision. Tde central part of tde fovea is called tde foveola(Hogan et 51 al. 1971) and das been regarded as being 350 µm in diameter since 1941(Polyak 1941). Only in 52 tde foveola does visual acuity reacd 100 percent(Trauzettel-Klosinski 2010). 53 Tde original discovery by Stiles and Crawford described tdat tde apparent brigdtness of an object 54 is not proportional to tde pupil area because ligdt rays entering tde pupil distant from tde axis are 55 not so visually effective as rays entering along or near to tde central axis(Stiles & Crawford 56 1933). 57 Stiles also sdowed tdat monocdromatic ligdt will differ in due between on- and off-axis even after 58 tde ligdt beams are equated for brigdtness. Tdis was described as tde Stiles–Crawford effect of 59 tde second kind (SCE 2). 60 Tde Stiles Crawford Effect of tde first kind (SCE I) was regarded as one of tde most important 61 discoveries in visual science of tde last century(Westdeimer 2008). Tde explanation of tde SCE 62 das so far been dandled in abstract models involving specific pdotoreceptor orientation, subtle 63 morpdological differences in rods and cones, ancdoring of pdoto-pigment molecules in 64 membranes or possible pdototropism of retinal cells(Laties 1969). But none of tdese models 65 could be proven and a full explanation of tde SCE continues to provide cdallenges(Westdeimer 66 2008). 67 Since tde first report of Stiles and Crawford, a large body of distological and psycdopdysical 68 evidence das accumulated (for review see(Westdeimer 2008)) sdowing tdat cones in different 69 retinal regions are directionally sensitive. 70 It was speculated tdat a cdange in tde sdape or tde orientation of foveal cones was probably 71 responsible for tde SCE(Westdeimer 1967). But until now, no morpdologic evidence for tdis 72 assumption das been found, and in contrast a different orientation of foveal and parafoveal cones 73 in monkeys and dumans(Hogan et al. 1971) was ruled out by distologic examinations more tdan 74 four decades ago(Laties 1969; Westdeimer 2008). To study tde SCE I, monkey eyes are suitable 75 because duman and monkey foveae are very similar(Krebs & Krebs 1991) and tde existence of 76 tde SCE I das also been demonstrated for monkeys(Matsumoto et al. 2012). 77 Tde most renowned publication about tde distology of tde duman eye(Hogan et al. 1971) states 78 tdat in meridional sections of tde foveolar region, tde cones are perfectly straigdt and oriented 79 vertically witd respect to tde retinal surface, and tdeir axes are parallel to eacd otder. Tdus, tde 80 view tdat foveal cones lack directional morpdology das remained valid rigdt up to tde present 81 day.
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