A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina

Abstract

In this paper, we describe the embryonic origin and patterning of the planar mosaic array of cone photoreceptor spectral subtypes in the zebrafish retina. A discussion of possible molecular mechanisms that might generate the cone mosaic array considers but discards a model that accounts for formation of neuronal mosaics in the inner retina and discusses limitations of mathematical simulations that reproduce the zebrafish cone mosaic pattern. The formation and organization of photoreceptors in the ommatidia of the compound eye of Drosophila is compared with similar features in the developing zebrafish cone mosaic, and a model is proposed that invokes spatiotemporally coordinated cell-cell interactions among cone progenitors to determine the identity and positioning of cone spectral subtypes. -734-763-1166. e-mail: praymond@umich.edu Abbreviations used in this paper: NND, nearest neighbor distance. KEY WORDS: pattern formation, retinal development, cell fate, opsin gene, visual pigment Cone photoreceptors in zebrafish are organized in a precise mosaic arrayPhotoreceptors are highly specialized neurons with unique, differentiated features associated with detection of light and transduction of neural signals (Cohen, 1972;Dowling, 1987). The identity, distribution, and spacing of individual photoreceptor subtypes is an important developmental parameter that influences many properties of visual function, including the ability to detect stimuli over a large range of light intensities, define the limits visual acuity, mediate color vision, etc. Most vertebrates have multiple spectral subtypes of cone photoreceptors as well as a single type of rod photoreceptor. The predominant animal models used to investigate photoreceptor differentiation and maintenance are rodents, which have strongly rod-dominant retinas, so we know much more about the developmental mechanisms involved in formation of rod photoreceptors (Morrow et al., 1998;Cepko, 1999;Levine et al., 2000;Livesey and Cepko, 2001) and relatively less about cone photoreceptor development (Adler, 2000). Although the human retina is rod-dominant in the periphery of the retina, the macula, which is most critical for functional vision, is strongly conedominant. Thus, the failure of cone photoreceptors to develop properly or the subsequent loss of cone function in humans has the most severe consequences on visual abilities (Neitz and Neitz, 2000;Aiello, 2003;Ambati et al., 2003;Pacione et al., 2003).Cone photoreceptor development has been studied in a few animal models that have abundant cones in addition to rod photoreceptors, most notably primates (Bumsted et al., 1997;Sears et al., 2000), chicks (Bruhn and Cepko, 1996;Adler et al., 2001), and teleost fishes (Branchek and BreMiller, 1984;Larison and BreMiller, 1990;Raymond et al., 1995;Schmitt and Dowling, 1996). Unlike rod photoreceptors, which except in some amphibians all express the same visual pigment gene (rod opsin or rhodopsin), different subtypes of cone photoreceptors express different cone opsin ...

In ovo thyroxine exposure alters later UVS cone loss in juvenile rainbow trout

“…In mice, S-opsin (most closely related to salmonid SWS1) is the first to be expressed during development, followed by L-opsin (of the M/LWS class), and the three opsins in humans (SWS and two M/LWS family member) follow a similar developmental course (Wang et al, 1992;Xiao and Hendrickson, 2000;Lukáts et al, 2005). The ontogenetic pattern of rainbow trout (salmonid) opsin expression differs from that of other fish species (Raymond et al, 1995;Stenkamp et al, 1996;Bumsted et al, 1997;Raymond and Barthel, 2004). In goldfish, RH1 appears first, followed by LWS, RH2, SWS2 and SWS1 opsins (Raymond et al, 1995;Stenkamp et al, 1996).…”

An absolute interval scale of order for point patterns

“…Distance-based measures use either nearest neighbour or neighbours (as defined by a triangulation or other structure). Examples include: global mean nearest-neighbour distance [41], global variance of nearest-neighbour distances [18,42], mean of local variance of nearest-neighbours distances [43][44][45] and other measures of the dispersion of nearest-neighbour distances [45]. Other distance-based approaches use all, rather than nearestneighbour, distances such as Ripley's L-function [46] and autocorrelation analysis [43,47,48].…”

Neurogenesis in the Fish Retina

“…This hypothesis will be discussed further in Section II.D. Regardless of the reasons for the fan gradient, this stereotyped, asynchronous pattern has been compared to the similarly asynchronous, posterior-to-anterior neurogenic wave of the Drosophila retina, and as such, has inspired a search for neurogenic mechanisms similar to those known for Drosophila (Raymond and Barthel, 2004;Stenkamp and Cameron, 2002). The fan gradient has also served as an important experimental tool in pursuing these and other mechanisms behind the neurogenic waves.…”

“…An additional interpretation is that cell fate may be dependent upon cell position during neurogenesis. Mechanisms that regulate cell fate based upon cell position are well described for Drosophila retinal neurogenesis, and so this interpretation has fueled the search for conserved mechanisms in vertebrates (Raymond and Barthel, 2004;Stenkamp and Cameron, 2002). The precise cone mosaic of the zebrafish has served as an assay for potential roles of signaling factors in regulating cone cell fate, since any factor that influences cone fate will theoretically disrupt the cone mosaic (Bernardos et al, 2005;Prabhudesai et al, 2005).…”