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Foveal regions of bird retinas correlate with the aster of the inner nuclear layer.

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THE ANATOMICAL RECORD 223:342-346 (1989)
Foveal Regions of Bird Retinas Correlate With the
Aster of the Inner Nuclear Layer
OSCAR INZUNZA, HERMES BRAVO, AND RICARDO L. SMITH
Departamento de Anatomia, Escuela de Medicina, Pontificia Unioersidad Cat6lica de Chile,
Santiago, Chile (0.1,H.B.) and Departamento de Morfologia, Escola Paulista de Medicina,
Sao Paulo, B r a d (R.L.S.)
ABSTRACT
A radiate specialization, the aster, has been found in whole-mount
retinas of birds and is associated to each one of the temporal and nasal fovea, with
the one related to the convexiclivate nasal fovea more evident. This radial arrangement extends uniformly in all directions from the foveal pit. Transverse sections of
the retina show that this structure is formed by bands of cells and bundles of fibers
from the inner nuclear layer.
The vertebrate retina is a comdex structure with different regional specializations i;l its cellular elements.
For example, in birds some topographic arrangements
are recognized in the retina both at the level of the
ganglion cell layer and in the nasal and temporal areas
and also in the horizontal stre* (Walls, 1942; Polyak,
1957; Ehrlich, 1981; Binggeli and Paule, 1969). These
specialized zones include, in some species, the presence
of foveas and have been related to the highest visual
resolution. Some evidence indicates that these retinal
zones project differently to the thalamocortical and to
the tectofugal pathways (Bravo and Pettigrew, 1981;
Bravo and Inzunza, 1983). Additionally, other topographic arrangements have been described in the outer
and inner nuclear layers of the pigeon retina, where a
high density of neurons has been described in the dorsal
area of the retina (red field) and in the nasal fovea
(Galifret, 1968). Recently, Morris (1982) described a different topographic structure, the aster, which is formed
by a columnar placement of the cells of the inner nuclear
layer in the retina of the chicken and states that the
central point, or node, of this structure probably coincides with the area of higher ganglion cell density of the
afoveal central area described by Ehrlich (1981). However, this possibility is undocumented.
To find the central area of afoveate retinas of birds, it
is mandatory to quantify the ganglion cells and to trace
their isodensity maps (Ehrlich, 1981; Bravo and Pettigrew, 1981). This procedure is better accomplished by
staining only the ganglion cell layer, but to do so obviously misses the location of the aster at the inner
nuclear layer.
In some animals it is known that central areas have
developed foveas, specializations with the highest density of receptors and ganglion cells (Fite and RosedieldWessels, 1975; Bravo and Pettigrew, 1981; Inzunza,
1986). To demonstrate the possible correlation between
these two different mecializations of the retina (the aster and the central area) and, taking advantage of the
fact that some raptorial birds have one or two wellin each eye, the present study investigated the Presence of the retinal aster, correlating its
location with the nasal and temporal foveal areas.
0 1989 ALAN R. LISS, INC.
MATERIALS AND METHODS
Retinas of the black vulture (Coragyps atratus) chimango caracara (Miluago chimango), burrowing owl
(Speotyto cunicularia), great horned owl (Bubo uirginianus), sparrow hawk (Falco sparuerius), and Chilean
eagle (Buteo fuscences australis) were studied.
After a period of dark adaptation to facilitate the removal of the pigment layer of the retina, the birds were
anesthetized with ketamine hydrochloride (HC1)(20 mgl
kg) and perfused through the heart with saline, followed
by 10% formalin. First, the eyes were detached and
opened by an encircling cut a t the level of the ora serrata. Then the vitreous was removed and the posterior
cup of the eye placed in 10% formalin or 2.5% glutaraldehyde in phosphate buffer. After cutting the optic nerve
under the pecten, the retina was carefully detached from
the pigmented layer and, once isolated, was mounted on
a gelatinized slide to get a whole mount with its vitreous
side up, dried at room temperature, defatted, and stained
with 0.2% cresyl violet (Bravo and Pettigrew, 1981)until
the inner nuclear layer cells became evident. Two retinas of C. atratus were trimmed; segments of foveal and
peripheral retina were fixed in 2% glutaraldehyde, in
phosphate buffer (pH 7.21, dehydrated, and embedded in
araldite; sections in a transverse plane of 1to 2 pm were
cut and stained with blue I1 and methylene blue.
RESULTS
In all the whole-mount retinas studied, a radial arrangement, or aster, was found when focusing on the
slide at the level of the inner nuclear layer. In the
bifoveate species, such as the one represented by Buteo
and Falco, we observed that this radial arrangement
was associated with each of the foveas, and that the
nasal aster was more evident than the temporal one
(Fig. 1).In the monofoveate species, as exemplified by
Coragyps, Miluago, Speotyto, and Bubo, as well as in
Received February 2, 1988; accepted July 22, 1988,
Address reprint requests to Oscar Inzunza, Departamento de Anatomia, Escuela de Medicina, Pontificia Universidad Catolica de Chile,
Casilla 114-D,Santiago, Chile.
FOVEAL ASTER IN BIRDS
343
Fig. 1. A Photomontage of the nasal fovea. B: Temporal fovea from the same retina of Fuko sparuerius.
Arrows show the rays of the aster converging toward the fovea CF). Cresil violet stain. Scale bar = 50 pm.
bifoveate animals, the aster was centered around the
fovea. The radial character of this structure, which is
formed by cellular bands alternated with bundles of
nerve fibers, extends from the border of the foveal pit to
as far as 1,500 pm (Fig. 2).
Transverse sections of the foveal region (Fig. 3) show
that cellular elements of the inner nuclear layer are
tilted from the center to the lateral aspects of the fovea.
In these sections it can be seen that bipolar cells, located
according to Galifret (1968)in the outer part of this layer
between the horizontal and Muller cells, are ordered in
cellular columns that are separated by bundles of fibers
of the inner nuclear layer cells. Toward the sides of the
fovea, these columns are oriented obliquely with respect
to the retinal surface in such a way that they generate
a symmetric arrangement around the fovea. The cellular columns range away from the fovea between the
outer (scleral) and the inner (vitreal) parts of this layer.
The Muller cells maintain a perpendicular arrangement
with respect to the retinal surface (Fig. 3).
DISCUSSION
The major finding of this study has been to show the
presence of a radial arrangement, the aster, of the cellular element of the inner nuclear layer around foveal
areas of the retina in several raptorial birds.
Whereas in the peripheral retina the receptor, bipolar,
and ganglion cells somata are all oriented perpendicular
to the retinal surface, in the foveal regions of the retina,
the same neurons have a n oblique orientation that is
clearIy shown in the transverse sections of the retina.
This oblique arrangement, especially that of the bipolar
cells, also has been observed in the retinas of lizards
(Makaretz and Levine, 19801, which points to the fact
0. INZUNZA ET AL.
344
T
2
b
D
L
Fig. 2. A Photomontage of a retinal whole mount from Coragyps
atratus nasal fovea. The aster was focused in the inner nuclear layer.
The rays of this structure extend from the border of the foveal pit (F)
in all directions (arrows).Cresil violet stain. Scale Bar = 200 microns.
The inset shows a higher magnification of this specialization, in which
the cellular bands (arrow) are separated by bundles of fibers. Scale bar
= 40 pm. B: Ganglion cell density map of the retina shown in A.
Numbers indicate neuronal density in thousands of cells per mm2. The
white dot represents the pit of the nasal fovea. The external border of
the black area and the inner line around the fovea represent densities
of 25,000 and 20,000 cells/mm2, respectively. The temporal afoveate
area (16,000 ceIls/mm2) did not show a n aster detectable in the whole
mount preparation. T = temporal; S = superior. Scale bar = 5 mm.
FOVEAL ASTER IN BIRDS
345
Fig. 3.Thin transverse section of the Corugyps atratus nasal fovea.
On both sides of the fovea, the oblique position of the bipolar cells
(solid arrows) can be seen; the open arrow shows the Muller cells,
which are perpendicularly oriented with respect to the retinal surface.
G = ganglion cell layer, I = inner nuclear layer, 0 = outer nuclear
layer. Blue II and Methylene Blue stain. Scale bar = 50 pm. Inset
shows a higher magnification of oblique oriented bipolar cells (arrow)
and bundles of fibers in the inner nuclear layer. Scale bar = 20 pm.
that in convexiclivate foveas the axis joining the receptor, bipolar, and ganglion neurons forms a more oblique
chain so that not only the pedicle of the receptor is more
laterally displaced with respect to its outer segment, but
the bipolar cells are obliquely oriented as well. For example, Makaretz and Levine (1980) have reported that
displacement of the receptor’s pedicle, from its outer
segment in the nasal fovea of the lizard Anolis carolinensis, is as much as 300 pm. Similarly, the displacement of bipolar cells is as much as 150 pm peripheral to
their parafoveal site of origin. Our data also show a
receptor bipolar and ganglion cell axis that is obliquely
oriented in the nasal fovea of birds. For example, in the
black vulture, bipolar displacement of the vitreal terminal has shifted as much as 300 pm from its scleral
parafoveal site of origin. This bipolar displacement is
less marked in the concaviclivate foveas (Maraketz and
Levine, 1980) and hardly perceptible in the afoveate
area centralis (Morris, 1982).
The first description of the aster was by Morris (1982)
in whole mounts and especially in tangential sections
from the afoveate chick retina, suggesting that the node
of this structure probably lies within the central area
reported by Ehrlich (19811, the area with the highest
density of ganglion cells. The present study demonstrates that in raptorial birds the aster correlates precisely with the foveal areas of the retinas, which are
known to have the highest density of neurons not only
in the ganglion cell layer, but also in the outer and inner
nuclear layer (Fite, 1973; Fite and Rosenfeld-Wessels,
1975; Bravo and Pettigrew, 1981).
Polyak (1957) showed that in macaques a radiate
structure in the temporal fovea of the retina was formed
by bundles of fibers of the outer plexiform layer corresponding to the inner cone fibers. The radiate structure
in the fovea of birds is formed by a columnar arrangement of cell bodies and fibers in the inner nuclear layer.
The radiate structure that Polyak (1957) observed in
the outer plexiform layer in the monkey seems to be the
same as that we observed in birds, but in this case it
extends as far as the inner nuclear layer. This anatomic
feature might be explained by the conspicuously high
density of neurons present in the foveal regions of birds,
especially at the inner nuclear layer (Fite, 1973). For
example, Fite and Rosenfeld-Wessels (1975) found that
in some species of bifoveate birds, such as the goshawk,
the number of receptors and ganglion cells around the
foveas is double the amount of the same cells found in
the rhesus monkey foveal area. As a result, the bipolar
cells that connect the receptor to the ganglion cell (Polyak, 1957) and also present a very high density, are
somewhat pulled away from the center of the fovea,
forming a radiate structure. This radiate structure is
more evident when the number of cells pulled away is
greater. This is the case for the nasal aster in Buteo
fuscences and Falco sparuerius, in which the number of
346
0. INZUNZA ET AL
ganglion cells around the nasal fovea is at least 20%
more than that found in the temporal fovea; consequently, this also occurs at the level of the inner nuclear
layer (Inzunza and Bravo, unpublished observations).
The radial arrangement of the inner nuclear layer,
found in close correlation with the nasal and temporal
foveas of birds, parallels the regional specializations described in the outer nuclear layer and the ganglion cell
layer. These features appear most like the anatomical
correlate of the functional channels found in these areas
of the retina and are related to the higher visual resolution in the binocular fixation by the temporal fovea or
in the monocular tracking of a prey by the nasal fovea
(Pettigrew, 1978).
Morris (1982) states that the aster of chicken embryos
is visible in retinas a t about 16 days’ incubation. On the
other hand, it is known that on day 14 of incubation, the
first synaptic structures appear in the plexiform layers
(Shefield and Fishman, 1970). Additionally, mitotic activity in the central retina of the chicken ceases prematurely on about day 8 of incubation, with the bipolar
and Miiller cells the last to complete their cycle of cellular activity (Kahn, 1974). These studies, when taken
together, suggest that the formation of the aster is
closely related to the establishment of synaptic contacts
of the bipolar cells in the retina.
ACKNOWLEDGMENTS
The authors thank Dr. F. Torrealba for helpful comments during the preparation of the manuscript. This
study was supported by Direccion de Investigacion, Pontificia Universidad Cat6lica de Chile, Grant 107/87. M.
Estrella Palacios typed the manuscript.
LITERATURE CITED
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aspects of the optic nerve and ganglion cell layer. J. Comp. Neurol.,
137:l-18.
Bravo, H., and J.D. Pettigrew 1981 The distribution of neurons projecting from the retina and visual cortex to the thalamus and tectum
opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto
cuniculuria. J. Comp. Neurol., 199419-441.
Bravo, H., 0. Inzunza 1983 Estudio anat6mico en las vias visuales
paralelas en Falconiformes. Arch. Biol. Med. Exp., 16t283-289.
Ehrlich, D. 1981 Regional specialization of the chick retina as revealed
by the size and density of neurons in the ganglion cell layer. J.
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Fite, K.V. 1973 Anatomical and behavioral coirelates of visual acuity
in great horned owl. Vision Res., 13:219-230.
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avian foveas. Brain Behav. Evol., 1297-115.
Galifret, Y. 1968 Les divers aires fonctionnelles de la retine du Pigeon.
Z. Zellforsch, 86.535-545,
Inzunza, 0. 1986 Distribucion de las celulas ganglionares en la retina
de Coragyps atratus. M. Sc. Thesis, Department of Morphology.
Escola Paulista de Medicina. Sao Paulo, Brasil.
Kahn, A.J. 1974 An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev. Biol.,
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Makaretz, M., and R. Levine 1980 A light microscope study of the
bifoveate retina in the lizard anolis carolinensis: General observations and convergence ratios. Vision Res., 20:679-686.
Morris, V.B. 1982 An afoveate area centralis in the chick retina. J.
Comp. Neurol., 210:198-203.
Pettigrew, J.D. 1978 Comparison of the Retinotopic Organization of
the Visual Wulst in Nocturnal and Diurnal Raptors, with a Note
on the Evolution of Frontal Vision. In: Frontiers in Visual Science.
S. Cool and E. Smith, eds. Springer, New York, pp. 328-335.
Polyak, S. 1957 The Vertebrate Visual System. The University of
Chicago Press, Chicago, pp. 213-285.
Sheffield, J.B., and D.A. Fischman 1970 Intercellular junctions in the
developing neural retina of the chick embryo. Z. Zellforsch.,
104:405-418.
Walls, G.L. 1942 The Vertebrate Eye and Its Adaptative Radiation.
Bloomfield Hills, Cranbrook Press, Michigan, pp. 187-190.
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