The anatomy of the foveola reinvestigated

Abstract

ObjectiveIn 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.MethodsSerial 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.ResultsIn 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° causes a very bright spot after passing through this area. However, when the angle of the light beam is changed to 10°, 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° 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.ConclusionWe show that unique cones and Müller cells with light fibre-like properties are present in the center of 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 foveolar cones of monkeys are not straight.

Glia of the human retina

“…the filaments are arranged along the light path through the cells (Reichenbach & Bringmann, 2010). these processes are pale which supports the light transmission through the tissue Reichenbach & Bringmann, 2010;Syrbe et al, 2018;Tschulakow et al, 2018;Yamada, 1969). In addition, in individuals with a v-shaped ONL in the foveola, the centralmost foveola contains only few, loosely scattered photoreceptor cell somata (Figure 10b); here, the centralmost foveola is predominantly filled by pale Müller and cone cell outer processes (Figure 12b, c,g) .…”

“…In addition, the cytoplasm of the processes of Müller cells of the foveal walls, which enwrapp the somata and outer processes of the central cone cells, is pale (Figure c,g). Near the OLM, the cytoplasm of Müller cell processes has a watery appearance (Figure c,f) (Nishikawa, ; Tschulakow, Oltrup, Bende, Schmelzle, & Schraermeyer, ; Syrbe et al, ). In contrast, Müller cells in the foveal walls and Müller cell somata and processes in the inner layer of the foveola (Figure e,f) have a dark cytoplasm.…”

“…The foveal pit was formed to improve the light transmission through the thick central retina (which contains high cell and synapse densities) to the central photoreceptors which provide the highest visual acuity. In addition to the centrifugal displacement of the inner retinal layers, which reduces the level of intraretinal light scattering (in OCT images of the central fovea, light reflection is visible only in the thin inner layer of the foveola; Figures a, b1, and a), and the elongation of the central photoreceptors which shortens the light path through the tissue (Figures a and b), the light transmission through the foveola is improved by further structural adaptations: (a) the plait of the thin inner processes of foveolar Müller cells (Figure d,e) creates a smooth transparent plate to avoid image distortions resulting from light refractions at uneven surfaces; (b) the basal lamina of the ILM and the inner processes of the foveolar Müller cells are very thin, with thicknesses far below the wavelength range of visible light (Figure d,e), likely to avoid light scattering; and (c) the decrease of the optical density of the cytoplasm of the outer Müller cell processes in the course from the cell somata to the OLM (Figure c,f) may be associated with an alteration of the cytoplasmic refraction index; these processes are pale which supports the light transmission through the tissue (Bringmann et al, ; Reichenbach & Bringmann, ; Syrbe et al, ; Tschulakow et al, ; Yamada, ). In addition, in individuals with a v‐shaped ONL in the foveola, the centralmost foveola contains only few, loosely scattered photoreceptor cell somata (Figure b); here, the centralmost foveola is predominantly filled by pale Müller and cone cell outer processes (Figure b,c,g) (Bringmann et al, ).…”

“…In addition, in individuals with a v‐shaped ONL in the foveola, the centralmost foveola contains only few, loosely scattered photoreceptor cell somata (Figure b); here, the centralmost foveola is predominantly filled by pale Müller and cone cell outer processes (Figure b,c,g) (Bringmann et al, ). It was shown that only light which hits perpendicularly the foveola causes a bright illumination of the central photoreceptors (Tschulakow et al, ). In dependence on the angle of the incident light, less light is transmitted through the Müller cell cone to the photoreceptors; this is likely a cause of the Stiles‐Crawford effect (Tschulakow et al, ).…”

“…It was shown that only light which hits perpendicularly the foveola causes a bright illumination of the central photoreceptors (Tschulakow et al, 2018). In dependence on the angle of the incident light, less light is transmitted through the Müller cell cone to the photoreceptors; this is likely a cause of the Stiles-Crawford effect (Tschulakow et al, 2018).…”