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Retinal Growth in Foveated Teleosts: Nasotemporal Asymmetry Keeps the Fovea in Temporal Retina

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Retinal Growth in Foveated Teleosts: Nasotemporal Asymmetry Keeps the Fovea in Temporal Retina The Journal of Neuroscience, June 1992. 12(6): 2381-2392 Retinal Growth in Foveated Teleosts: Nasotemporal Asymmetry Keeps the Fovea in Temporal Retina Stephen S. Easter, Jr. Department of Biology, University of Michigan, Ann Arbor, Michigan 48109-1048 and Vision, Touch, and Hearing Research Centre, Department of Physiology and Pharmacology, University of Queensland, Brisbane, QLD 4067, Australia Fish retinas continue to grow throughout life by adding neu- the inflation of the eye, and active, as new cells are added. Rods rons at the margin, with the result that cells born at a pe- are added interstitially throughout the retina (Johns and Fer- ripheral site are steadily displaced toward the center of the nald, 1981; Raymond and Rivlin, 1987) but all the other cell enlarging retina. This presents a functional problem for fish types are added at the margin, where stem cells proliferate to with specialized temporal areas such as a fovea-how to produce more stem cells and postmitotic neuroblasts (Muller, reconcile continual growth with the maintenance of a tem- 1952; Hollyfield, 1972; Johns, 1977). The stem cells continue poral location for the fovea. One possibility is that the retina to proliferate on the margin; the postmitotic cells remain just grows asymmetrically, with most new retina added nasally, inside it, and differentiate into the various types of retinal neu- relatively little temporally. ron. The new neurons thus form an annulus around the edgeof I have tested this hypothesis by evaluating retinal growth the eye, central to the marginal germinal zone from which they in marine teleosts from 15 families, both foveated and un- recently emerged,and peripheral to the preceding generation of foveated. The pattern of growth was revealed by exploiting neurons (Scholes, 1979; Rusoff and Easter, 1980). the fact that each new generation of ganglion cells sends Such appositional addition of new annuli provides an inter- its axons into the optic nerve as a cohort; small grains of esting complication for vision, In goldfish, for example, the eyes the carbocyanine dye 1 ,l’-dioctadecyl-3,3,3’,3’-tetramethyl- of large and small fish are conformal; in both, the retina subtends indocarbocyanine were applied to various sites in the cross the samevisual angle, about half of a hemisphere,and the optic section of the optic nerves of adults, and the retrogradely disk lies approximately at the center (Easter et al., 1977). These labeled cell bodies in the retina were visualized in whole- facts, coupled with the annular mode of cell addition, imply mounts. The labeled cells lay in annuli, each one a generation that as the eye grows, the receptive fields of retinal neurons must of ganglion cells. continually move from the periphery toward the center of the Representatives of seven of the families showed clearly retina’s visual field. For instance, a ganglion cell born on the asymmetric growth: the labeled annuli were close together temporal margin would initially have its receptive field in front on the temporal side and more distant nasally, the embryonic of the fish, but as new cells are added to the margin, this same fissure curved from its ventral origin toward the temporal cell’s receptive field would shift laterally and posteriorly. How side, and in six of these families, labeled fibers from tem- the brain managesthis ever-changing relationship with the out- poral retina skirted the fovea. Members of the other eight side world is completely unknown, but the problem is slightly families, without specialized areas, had more symmetric ret- simplified by the fact that the goldfish retina lacks a specialized inal growth: labeled annuli were equally spaced on all sides, urea; that is, a region of high cell density (RHCD) (Johns and the embryonic fissure was vertical, and there were no skirt- Easter, 1977). Becausecell density varies relatively little with ing fibers. position, one part of the retina is probably functionally equiv- The following hypothesis is supported: the retina grows alent to another, and the retinal modules that are added at the asymmetrically, and maintains the area for acute vision ori- edge resemblethose everywhere elsein the retina. ented toward the anterior field. The problem of reconciling annular growth with vision is more complicated in those fish with an RHCD. Walls (1942, p The retina of a teleost fish grows throughout much of the ani- 304) lists 24 teleost species,from 13 genera, that have a fovea mal’s life (Muller, 1952; Johns and Easter, 1977; Meyer, 1978). (an RHCD marked by a pit in the inner limiting membrane), The enlargement is both passive, as the retina is stretched by and notes that many others have areue that are RHCDs not associatedwith a pit (for examples, see Collin and Pettigrew, 1988a,b). Presumably these RHCDs-fovea or area-are spe- Received Dec. 4, 199 1; accepted Jan. 16, 1992. cialized for high resolution (Collin and Pettigrew, 1989), as in This work was carried out while on sabbatical leave at the Vision, Touch, and the human eye. The fish fovea differs structurally from the hu- Hearing Centre, with support from the Australian Research Council and NIH man fovea, however, in that it has all the retinal layers present Research Grant EY-00168. I thank Prof. Jack Pettigrew, Dr. David Vaney, and others at the Centre for their help and hospitality. I thank Ms. Rita Collins and except that of the optic fibers. The ganglion cell layer lies at the Celeste Malinoski for doing the histology, and Drs. David Cameron, Peter Hitch- bottom of the pit, the walls of which are formed by the mounded cock, Jack Pettigrew, Pamela Raymond, John Scholes, Steve Wilson, Ms. Riva optic axons. Marcus, and Mr. John Burrill for their comments on the manuscript. Correspondence should be addressed to Stephen S. Easter, Jr., Department of In almost all fish that have one, the RHCD is in far temporal Biology, University of Michigan, Ann Arbor, MI 48 109- 1048. retina, and this location is vulnerable to the effects of annular Copyright 0 1992 Society for Neuroscience 0270-6474/92/122381-12$05.00/O growth. How can a temporal RHCD remain temporal, and avoid 2382 Easter - Asymmetric Retinal Growth Table 1. Types of fish examined in this study, grouped according to et al., 198 l), so if a smallquantity of retrogradetracer is appliedto a whether the retina grew symmetrically or asymmetrically (see Results) fascicle, an annulus ofganglion cells is labeled (Rusoff and Easter, 198 1). Most of the fish described below had ribbon-shaped optic nerves (Tapp, 1973; Anders and Hibbard, 1974), in which sequential generations of Symmetric growth axons are laid out linearly along the ribbon, oldest at the central end, 1. Acanthuridae (surgeon fish) youngest at the peripheral (ventral) end (Scholes, 1979). Thus, it was a. Purucun~hurus hepatus (blue tang) (1) possible to apply tracer at a particular site in the cross section of the 2. Blenniidae (blennies) nerve and predict the approximate retinal location of the labeled cells. a. Sulurius sinuosus (fringelip blenny) (2) Fish were obtained by netting at the Heron Island Research Station b. Zstiblennius edentulu (rippled rockskipper) (2) on the Great Barrier Reef, in a trawl on Moreton Bay, and by purchase 3. Chaetodontidae (butterfly fish and coral fish) from a local pet store. Individual fish were anesthetized by immersion a. Chelmon rostrutus (beaked coral fish) (2) in a 0.1% solution of tricaine methane sulfonate, and after the aorta 4. Gobiidae (gobies) was cut, both eyes were removed with a stump of the optic nerve at- a. Buthygobiusfuscus (common goby) (2) tached. The cornea, lens, and iris were removed, and the fish’s standard 5. Mullidae (goatfish) length and lens diameter were recorded. Both eye cups were fixed by a. Upeneus trugulu (freckled goatfish) (2) immersion in 2% or 4% paraformaldehyde in 0.1 M phosphate buffer 6. Opistognathidae Cjawfish) at room temperature for 4 hr to 2 weeks. The dye l,l’-dioctadecyl- a. Unidentified (1) 3,3,3’,3’-tetramethylindocarbocyanine (DiI; obtained from Molecular 7. Pomacentridae (damselfish) Probes) (Honig and Hume, 1986), which diffuses in the plasma mem- a. Duscyllus uruanus (humbug dascyllus) (1) brane in fixed tissue (Godement et al., 1987), was applied to one or b. Chrysiptera unimuculatu (one-spot damselfish) (1) more sites on the optic nerve stumps, or intraretinally, and the tissue 8. Syngnathidae (pipe fish and sea horses) was returned to fix at 37°C. After a suitable interval (4 d to 2 weeks, a. Truchyrhumphus bioarctutus (short-tailed pipefish) (1) determined by examining the intact tissue in a fluorescence microscope), b. Hippocampus kudu (spotted sea horse) (1) the tissue was prepared for whole-mounting. The retina and adherent c. Unidentified (sea horse) (1) pigmented epithelium were dissected away as a unit from the rest of Asymmetric growth the eye, relaxing cuts were made to allow it to lie flat, and it was mounted 1. Callionymidae (dragonets) with the inner limiting membrane up, in 50% phosphate buffer, 50% a. Unidentified (3) glycerol, and coverslipped. The intersection of the embryonic fissure 2. Cirrhitidae (hawkfish) with the margin was taken as the ventral pole, and all whole-mounts a. Cirrhitichthys falco (dwarf hawkfish) (1) are shown with the ventral pole below, the dorsal pole up, and the 3. Iabridae (wrasses) nasotemporal axis horizontal. Some eyes were embedded in glycomethacrylate, sectioned, and stained a. Mucropharygodon negrosensis (black wrasse) (1) 4. Monacanthidae (leatherjackets) with toluidine blue. a. Unidentified (8) Slides were viewed and photographed on a Zeiss Universal compound 5. Pinguipedidae (sand perch) microscope with rhodamine-cube epiillumination. Table 1 lists the 15 teleost families, and where possible the genera a. Parupercis cylindricu (sharpnose sand perch) (4) b. Purupercis nebulosu (barred sand perch) (10) and species, included in this study.
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