2
Development of the Foveal Specialization
Keely M. Bumsted O’Brien
CONTENTS
INTRODUCTION
FOVEAL DEVELOPMENT
CONCLUSIONS AND PERSPECTIVES
REFERENCES
INTRODUCTION
“Vision is the foundation of intelligence and the chief source of our knowledge”[1]. Vision, our primary sensory modality, is supported by a complex anatomy and physiology that coordinates the interpretation of and interaction with our world. The initial steps in seeing begin in the retina, where the processing of important features such as color, form, and movement is initiated. These functions are mediated by interactions between a great diversity of cell types in the retina, the three glial and six major neuronal cell classes. The approximately 55 distinct retinal cell types are each nonrandomly distributed across the retina to maximize retinal coverage and are organized in characteristic topographic patterns. The most highly specialized area of our retina, which is also the focal point of cell topography, is located at the center of gaze in a region known as the macula leutea or macula. Within the macula is a morphologically distinct region called the fovea Centralis or fovea, which is responsible for the most acute color, spatial, and temporal visual resolution properties in primates [1–4].
The fovea is defined as a small anatomical pit or depression in the retina at the center of gaze; it lacks rod photoreceptors and has the highest density of cone photoreceptors. In humans, the fovea is responsible for our high visual acuity, measured to be 6/6 (20/20 or approximately 30 cycles per degree). Among mammals, the presence of a fovea is restricted to primates; however, many other vertebrates, such as many birds, certain species of fish, and chameleons, have a fovea and enhanced visual acuity [5–10]. All foveae share the common feature of a retinal pit, although many other characteristics, such as pit depth, width, cell composition, and density, are variable between species. In general, bird and fish foveae are smaller in diameter with steeper walls, leading to the description of the these foveae as convexiclivate [7, 11]. In addition to being steeper, many other vertebrate foveae contain a continuous inner nuclear layer (INL) and ganglion cell layer
From: Ophthalmology Research: Visual Transduction and Non-Visual Light Perception
Edited by: J. Tombran-Tink and C. J. Barnstable © Humana Press, Totowa, NJ
17
18 |
Bumsted O’Brien |
(GCL) across the center of their pit, whereas these layers are missing in the human fovea [10]. In the pigeon (Columba livia), northern blue jay (Cyanocitta cristata), and ostrich (Struthio camelus) the fovea is shallower compared to the human, although visual acuity is close to, but slightly poorer than, human acuity under comparable conditions (approximately 16–20 cycles per degree) [10, 12–16]. Only the large birds of prey such as the wedge-tailed eagle (Aquila audax; 140 cycles per degree) have a higher visual acuity compared to primates. This increased acuity is likely based in the higher foveal cone density and has been suggested to be optically augmented by the steep structure of the pit [10, 13, 17].
The primate fovea is located in the center of the macula, an oval 1.5-mm wide yellow spot visible while viewing the fundus. The yellow color of the macula lutea is due to the presence of the carotenoid pigments lutein and zeaxanthin. Within the macular region lies the fovea (Fig. 1A, circle). The morphological features of the human fovea are characterized by a pit 600–800 m wide that is lacking inner retinal neurons, blood vessels, and rod photoreceptors but contains the highest density of cones in the retina (Fig. 1B, bracketed region). Maximum foveal cone densities range from between about 100,000 and 400,000 cones/mm2 in humans (Fig. 1D; [18–24]). The very center of the fovea, the foveola, is further specialized in that it contains long- (L) and medium- (M) wavelength specific cone density peaks, while short- (S) wavelength specific cones, which elsewhere comprise 8–10% of the cone population, are absent from the central 20 m of the foveola [3, 25]. Cone densities decline rapidly with eccentricity, such that even in the fovea there is a steep density gradient [20, 26]. Outside the region of high cone density, the edges of the fovea form a slope where the number of inner retinal neurons begins to increase as the foveal region gradually transitions to a fully layered retina at the rim margin (Fig. 1B, arrowheads). The retinal capillary network is present on the foveal rim but not on the foveal slope. The foveal rim is also distinguished by an accumulation of cells in the GCL and the INL [1, 2, 10, 26–28].
The accumulation of retinal ganglion cells on the foveal rim is correlated with the high density of cone photoreceptors in the foveal center (Fig. 1D) because each foveal cone stimulates two midget ganglion cells (i.e., one ON and one OFF). Each ON or OFF midget ganglion cell receives information from a single cone through an ON or OFF bipolar cell, respectively (Fig. 1C) [1, 29–31]. This dedicated line of information flow and the small size of the ganglion cell arbors and receptive fields in the central retina mean that individual foveal cones represent one small region of spatial information that is transmitted to the parvocellular layers of the dorsal lateral geniculate nucleus with little information loss (reviewed in [32]). Outside the fovea, there is a regular decrease in the density of cones, which is in parallel with the decrease in ganglion cell density and increased rod density (Fig. 1D). As the number of ganglion cells decreases, there is an increase in the size of ganglion cell dendritic arbors and receptive field sizes [33, 34]. Therefore, relative to the macular region, the peripheral retina has a greater summation of information due to the larger ganglion cell receptive field, lower cone densities, and increase in rod number [10, 20, 21, 35, 36].
The complex organization of the retina centered on the fovea is essential for our optimal visual functioning. When this topographical arrangement is compromised in the adult or during development, the result is poor vision. Almost a quarter of all adult
Development of the Foveal Specialization |
19 |
Fig. 1. Characteristics of the adult human fovea. A Fundus photograph of a human macular region. The circled region indicates where the foveal pit is located. B Cross section of the human fovea stained with cresyl violet. In the center of the fovea (bracket), all the inner retinal neurons have been pushed aside, and the cones are found at a high density. The edges of the pit (arrowheads) contain a high density of ganglion cells and are where the edges of the avascular zone are located. C Diagram of a foveal cone, ON and OFF midget bipolar cell and ganglion cell circuit. Note the long axon of the foveal cone. D Photoreceptor densities across the human retina (modified from [18]). Cones peak in the center of the fovea and then fall quickly into the periphery. Rods are absent in the foveal center and peak outside the fovea. GC ganglion cell, GCL ganglion cell layer, INL inner nuclear layer, OD optic disk, ONL outer nuclear layer.