Nasotemporal Asymmetry during Teleost Retinal
Growth: Preserving an Area of Specialization
Carol A. Zygar, Marc J. Lee, Russell D. Fernald
Program in Neurosciences and Department of Psychology, Jordan Hall, Bldg. 420,
Stanford University, Stanford, California 94305-2130
Received 10 February 1999; accepted 27 April 1999
ABSTRACT: Teleost fish retinas grow throughout
adult life through both cell addition and stretching. Cell
division occurs at the periphery of the retina, resulting
in annular addition of all cell types except rod photore-
ceptors, which are added in the central retina. Since
many teleosts have a region of high cellular density at
the temporal pole of the eye, we analyzed whether and
how this specialized region of high visual acuity main-
tained its relative topographical position through asym-
metric circumferential growth. To do this, we measured
the pattern of long-term retinal growth in the African
cichlid Haplochromis burtoni. We found that the retina
expands asymmetrically along the nasotemporal axis,
with the nasal retina growing at a higher rate than the
temporal, dorsal, or ventral retinae, whose growth rates
are equal. This nasotemporal asymmetry is produced
via significantly greater expansion of retinal tissue at the
nasal pole rather than through differential cell prolifer-
ation. The mechanisms responsible for this differential
retinal enlargement are unknown; however, such asym-
metric expansion very likely minimizes disruption in
vision during rapid growth. © 1999 John Wiley & Sons, Inc. J
Neurobiol 41: 435– 442, 1999
Keywords: teleost; fish; retina; asymmetry; growth;
RHCD
Although all vertebrate eyes share a similar structure
arising from common developmental programs, the
eyes of cold-blooded animals are unique because they
grow throughout life. For example, the eyes of teleost
fish enlarge in proportion to increasing body size into
adulthood through both stretching and cell addition
(Mu ¨ller, 1952; Lyall, 1957; Scholes, 1976; Johns and
Easter, 1977; Meyer, 1978). This ongoing cell addi-
tion occurs at two locations in the retina. Rod photo-
receptors exclusively are intercalated throughout the
central retina, arising from the division of precursor
cells in the outer nuclear layer (Johns and Fernald,
1981). All other cell types, including cone photore-
ceptors, are added at the marginal germinal zone
where the retina meets the iris. Since the physical
properties of light tightly constrain the structure of a
functioning eye (Fernald, 1988), its continuous
growth requires precise control. For these reasons, the
adult teleost eye has proven to be a useful model
system for analyses of retinal development and, more
generally, for study of central nervous system assem-
bly. A particularly useful fish because of its rapid
growth and predominant reliance on vision for social
communication and survival is the African cichlid
Haplochromis burtoni (Fernald, 1984).
Because of the lateral location of fish eyes, their
continued growth poses particularly complicated
problems, because images from the front of the ani-
mal fall near the edge of the temporal pole of the
retina. In H. burtoni, the temporal pole maintains a
fourfold greater density of cone photoreceptors than
the nasal pole of the retina throughout the life of the
animal (Fernald, 1983). All other cell types (e.g.,
bipolar, amacrine, and ganglion cells) except rods also
maintain this fixed density ratio between temporal and
Correspondence to: R. D. Fernald
Contract grant sponsor: NIH; contract grant number: EY 05051
Contract grant sponsor: Stanford Undergraduate Research Op-
portunity
© 1999 John Wiley & Sons, Inc. CCC 0022-3034/99/030435-08
435