Specialized photoreceptor composition in the raptor fovea

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Visual spatial resolution (or visual acuity) defines the detail that can be resolved in a visual scene. As in a camera, the spatial resolution of an eye is determined by the anterior focal length (hereafter, focal length) of the eye's optical system and the density of the light sampling units in the neural retina (Land & Nilsson, 2012). The larger the eye, the longer the focal length and the larger the image projected onto the retina. The denser the receptor sampling array, the more spatial detail can be extracted from the retinal image (Miller, 1979). Thus, in order to achieve high spatial resolution, an animal has to have a large eye with a dense photoreceptor array in the retina (Meyer, 1977).
Among all animals, Accipitriform and Falconiform raptors have the most acute vision that has ever been measured (Fischer, 1969; Reymond, 1985). Behavioral studies show that large raptors such as Old World vultures (Fischer, 1969) and wedge‐tailed eagles (Aquila audax) (Reymond, 1985) have twice the spatial resolution of humans (Land & Nilsson, 2012). These findings raise intriguing questions about the basis of enhanced spatial resolution in raptorial birds.
Despite having body sizes much smaller than that of humans, some birds of prey have eyes of equal or larger size (Martin, 1983; Reymond, 1985). These large eyes allow for a long focal length that results in a correspondingly large retinal image (Land & Nilsson, 2012). In addition, many birds have central or temporal regions in the retina with increased photoreceptor density (Meyer, 1977). These regions are referred to as "areae" and may or may not contain a fovea. The fovea is a region of the retina where photoreceptor densities are highest and other retinal layers are fully or partially displaced, resulting in a depression, which constitutes the "fovea" proper. Unlike human eyes, which have only one shallow central fovea, the eyes of many raptor species (as well as swallows, martins, terns, kingfishers, and some other birds; Moroney & Pettigrew, 1987; Rochon‐Duvigneaud, 1943) have two foveae: a deep central fovea that views the lateral visual field, and a shallower temporal fovea that views the frontal visual field (e.g., Oehme, 1964; Reymond, 1985).
To maximize visual acuity, the fovea should only contain photoreceptors contributing to high‐resolution vision. Rods cannot operate in the bright‐light conditions required for optimal foveal function (Snyder & Miller, 1977) and they are accordingly absent from the foveae of some species. For example, the primate fovea, including that of humans, is rod‐free (e.g., Finlay et al., 2008; Packer, Hendrickson, & Curcio, 1989) and the central areae or foveae of several bird species have been found to be rod‐free (Bruhn & Cepko, 1996; Coimbra, Collin, & Hart, 2015; Querubin, Lee, Provis, & O'Brien, 2009). Furthermore, to achieve highest image quality the eye needs to avoid chromatic aberration, which is most severe for the short wavelength light (for more detail please see Discussion). Probably for this reason blue‐sensitive cones are absent from the central‐most part of some primate foveae (e.g., Martin & Grünert, 1999; Wikler & Rakic, 1990) leaving only green and red‐sensitive cones for the tasks of highest acuity. These observations suggest that the demands of high‐acuity vision select for a specific photoreceptor complement in the fovea.
Birds are thought to utilize different subsets of their photoreceptor complement for specific visual tasks (Hart, 2001b). As in many other vertebrate taxa, rod photoreceptors mediate dim light vision.
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