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Scanning electron microscopy of monkey foveal photoreceptors.

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THE ANATOMICAL RECORD 205~363-37311983)
Scanning Electron Microscopy of Monkey Foveal Photoreceptors
BESSIE BORWEIN
Department ofdnatomy, University of Western Ontario, London, Ontario,
Canada N6A 5Cl
ABSTRACT
Rhesus monkey retina and especially the foveal photoreceptors (PR) were investigated by scanning electron microscopy (SEMI. There are
a few scattered SEM photomicrographs of the primate retina in the literature
but this is the first detailed and comprehensive view by SEM of a primate
retina. Some new aspects of surface morphology are displayed and the study
also highlights and emphasizes some aspects of photoreceptor structure that
have either been overlooked or not clearly displayed in studies using transmission electron microscopy only.
For examination by SEM retinas were fixed in glutaraldehyde-formaldehyde,
osmicated, immersed in thiocarbohydrazide, dehydrated in alcohols, and goldcoated. The fovea appears as a sharply defined pit with steep slopes, and its
vitreal surface looks different from that of the rest of the retina. It appears to
have a matted surface. The rest of the vitreal surface is relatively smooth and
displays distinct lines which diverge in a radiating pattern from the foveal
slopes. The choroid has a spongelike appearance; the sclera appears fibrous
with the fibers running parallel to the vitreal surface. Photoreceptor nuclei
are sometimes lost during tissue processing. They leave a discrete “nuclear
nest” formed from Muller cell processes. Henle fibers turn at a sharp angle
from the cones to run parallel to the vitreal surface. The external limiting
membrane is seen as a clear line. Immediatelv vitreal to it, the Miiller cell
microvilli surround the proximal inner segments. The cone inner segment
(CIS) narrows toward the cilium where the cell is markedly constricted. The
ciliary connectives are aligned and appear as a shadowy, slightly wavy zone
when the retina is viewed in vertical section. The freestanding, tapering
calycal processes (CP) arise from and are continuous with longitudinal CIS
ridges. CP surround the proximal parts of the outer segments (OS), but there
are no CP around the ciliary backbone. Some CP bear small protrusions. 0s
break off and remain embedded among the pigment epithelium microvilli
(PEM) more often than PEM remain attached to 0s distal ends. The foveal 0s
tapers slightly from its proximal to its distal end. The 0s may bear knoblike
swellings and convolutions in their more distal regions but not a t their tips.
There are very few SEM studies of normal
photoreceptors of monkey (Borwein et al.,
1980; Dickson et al., 1973; Kuwabara, 1970;
Smith and Finke, 1972; Wickham and Adams, 1979) and man (Breipohl et al., 1974b;
Follman and Radnot, 1979; Kuwabara, 1970;
Radnot, 1978; Wickham and Adams, 1979).
Very few good photographs are available.
Several of these studies provide only one or
two pictures (Breipohl et al., 1974b; Follman
and Radnot, 1979; Kuwabara, 1970; Radnot,
1978; Smith and Finke, 1972) and one is an
abstract without illustrations (Wickham and
Adams, 1979).
0 1983ALAN R. LISS, INC.
This paper presents details about monkey
foveal retinal ultrastructure as seen by scanning electron microscopy (SEMI that have
not been presented before, and it also corroborates and elaborates some aspects of primate photoreceptor morphology that have
been established by studies using transmission electron microscopy (TEM) (Cohen, 1963,
1972; Dowling, 1965; Dunn, 1973; Fine and
Yanoff, 1979; Hogan et al., 1971; Missotten,
1965; Young, 1969). It is the first extensive
Received April 20,1982; accepted November 11, 1982.
364
B. BORWEIN
view by SEM of a primate retina and enhances our visual conceptions of these structures. It extends our knowledge of primate
photoreceptors. It is specifically complementary to a previous TEM study of monkey
foveal photoreceptors by the author and coworkers (Borwein et al., 1980).
SEM provides photographs of photoreceptors that are not only striking but which also
emphasize details of surface morphology that
have been overlooked or underemphasized
when the three-dimensional picture depended wholly or mainly on mental reconstructions from small, thin sections. The
special advantage of the SEM is its depth of
focus over a relatively large area a t fairly
high magnifications.
Hollenberg, 1973; Dickson and Hollenberg,
1971; Leuenberger, 1971; Radnot, 19781, the
most commonly used procedure is aldehyde
fixative, usually followed by osmication, and
critical point drying. We have found that
thiocarbohydrazide (Malick et al., 1975) improved the cleanliness and clarity of the surfaces. “In spite of shrinkage, however, the
proportions, topography and integrity seem
to have been maintained extremely well”
(Lewis et al., 1969) compared with most of
the techniques used for preparation of materials for SEM.
All the animals were treated according to
the protocol specified in “Guide for Care and
Use of Laboratory Animals” (DHEW Publication No. NIH 78-23, 1978).
MATERIALS AND METHODS
Mature rhesus monkeys were first sedated
with Sernylan and then killed by injection of
Nembutal. The enucleated eyes were incised
at the ora serrata and immersed in cold fixative (2.5% glutaraldehyde + 0.5% formaldehyde in 0.1 M Sorensen’s or cacodylate buffer,
pH 7.4).
As fixation proceeded, the cornea, lens, and
vitreous were dissected away, in three successive stages, separated by 10-minute intervals. When the tissues were hardened (about
30 minutes) the fovea was removed with a
trephine. Total fixation time in aldehydes
was 1%hours at room temperature. The samples were rinsed in buffer, postfixed in 1%
buffered Os04 for 1% hours, washed in several changes of distilled water, immersed in
thiocarbohydrazide for 15 minutes (modified
from Malick et al., 19751, washed again several times, postfixed in 1%Os04 for 1 hour,
washed again and dehydrated in graded alcohols, critical point dried, coated with gold
(20 nm) in a Technics Hummer sputter coater, and viewed in a Philips SEM 501 or a n
Hitachi HHS-2R SEM a t 20 kV. Photographs
were taken on Kodak plus-X film.
A considerable degree of shrinkage occurs
in the preparation of tissue for SEM, estimated by Lewis et al. (1969) and Ali and
Wagner (1976) as about 30% greater than for
plastic-embedded material. Hansson (1970~)
tried several fixation methods and found that
he got the most reproducible results with
buffered glutaraldehyde and formaldehyde
but good results were also obtained with 1%
buffered osmium. I have surveyed the methods reported for SEM work and although airdrying was used (Antal, 1977; Borwein and
OBSERVATIONS
The fovea appears as a sharply defined pit
with steep slopes. The floor of the pit is covered by matted material and it differs in
appearance from that of the rest of the vitreal surface of the retina, where there is a
pattern of striations radiating from the foveal slope (Fig. 1).The narrowing of the retina
is clearly displayed where the inner layers
thin out in the fovea. The region of the “central bouquet of cones” (Rochon-Duvigneaud,
19431, the foveola, is seen a t the thinnest part
of the retina in the center of the fovea (Figs.
1, 2).
The apical surface of the pigment epithelium is covered by a dense mat of microvillous processes Figs. 1, 3). The retina easily
detaches from the pigment epithelium during tissue preparation and many outer segments break off and remain attached to the
pigment epithelium, embedded among the
microvillous processes (Fig. 3). Bruch’s membrane appears as a narrow, relatively homogeneous layer lying immediately below the
pigment epithelium on its scleral side (Figs.
2, 3). The choroid has a spongelike appearance (Figs. 2 , 3 ) and the broad sclera appears
fibrous with the fibers running approximately parallel to the vitreal surface (Fig. 2).
The nuclei of the foveal cones are seen to
be arranged in seven layers in Figure 4.Each
nucleus is closely surrounded by a “nuclear
nest,” which is known to be formed by Muller
cell processes (Borwein et al., 1980). Occasionally, when a nucleus is lost during tissue
preparation, it leaves a discrete, empty “nuclear nest,” with the inner and outer cone
fibers intact and in place (Fig. 4).
SEM OF MONKEY FOVEAL PHOTORECEPTORS
The long, inner cone fibers, which form the
Henle fiber layer of the fovea, turn at a very
sharp angle from the inner and outer segments (Fig. 4).The external limiting membrane (ELM) (formed by a series of junctional
complexes, zonulae adhaerentes, between
photoreceptors and Muller cells) appears as a
clear, thin line (Fig. 41,while the ciliary connectives are aligned and appear as a wider,
shadowy zone extending across the photoreceptors at their inner-outer segment junctions, more or less parallel to the ELM (Figs.
4-6). This zone is made more apparent also
because the inner segment tapers abruptly
at this level, where the cilium is apparent,
and there is thus more extracellular material
present.
Microvillous processes of Muller cells are
of variable lengths and they project beyond
the ELM to surround the most proximal (vitreal) parts of the inner segments of both rods
and cones. They can be seen faintly in Figure
4 and are well displayed in Figure 5.
The inner segment occupies the region between the external limiting membrane and
the ciliary connective. The cell is constricted
sharply at the region of the cilium, more
markedly so away from the foveal center, the
foveola (compare Figs. 5 and 7). The cone
inner segment is wider in the parafoveal
areas (Fig. 5) and it lengthens and narrows
toward the foveola (foveal center) where cones
only are present (Fig. 7). The rod inner segment and the foveolar cone inner segment
change comparatively little in shape and size
from the ELM to the ciliary zones (Figs. 5,7).
In the very center of the fovea, in the foveola,
the outer segments and inner segments are
in a straight line and they are parallel to
each other. On either side of these most central cones, the outer segments tilt slightly
away from their inner segments in the direction away from the central cones (Fig. 6).
The surface of the inner segment is longitudinally ridged and grooved (Figs. 5, 8, 10)
and some of these ridges bear small knobs
(Figs. 8, 10, 11).The ridges are most prominent a t the scleral ends of the inner segments and here they are seen to be
continuous with the freestanding calycal processes which appear to arise from the ridges
(Figs. 8, 10). The calycal processes surround
the vitreal ends of the outer segments. They
are broad where they originate, and they
taper. They vary slightly in length (Figs. 810).They are prominent and long in the cones
but extend for only a relatively short part of
the total cone outer segment length (Figs. 9,
365
11).One or two (more rarely, three) calycal
processes usually arise from one inner segment ridge (Figs. 8, 10).
The ciliary connectives are aligned in the
photoreceptors to form a shadowlike zone extending across the photoreceptors a t the cone
inner-outer segment junctions, where the
cells narrow (Figs. 3, 6, 7). The cilium has a
very irregular surface outline. Two or three
very short, stublike calycal processes are associated with it (Figs. 8,lO). In both rods and
cones the cilium extends to become the ciliary backbone which lies alongside the discs
on one side of the outer segment. There seems
to be no particular pattern in the arrangement of the photoreceptors with regard to the
positions of the cilia and ciliary backbones in
their relation to the discs. The orientation
seems random (Figs. 8, 10). There are no calycal processes around the ciliary backbone
(Figs. 8 , l O ) . When the outer segment breaks
off from the inner segment it does so above
the region of the ciliary connective whereas
the calycal processes often remain attached
to the inner segment and project above the
plane of the break (Fig. 11).
Often the cone outer segments are seen to
be irregular in outline, bearing nodules, or
they are folded on themselves, mainly in
their midregions and more distal parts. The
nodules and folds are found scleral to the
region of the calycal processes, but the distal
tip itself is never involved (Figs. 3,7,9, 11).
The long outer segments of the foveolar
cones are slightly narrower a t their tips than
they are immediately proximal to the cilium
(Figs. 7, 11).The foveal cones are elongated,
very closely packed together, and their inner
and outer segments are of approximately
equal lengths. There is a slight taper in the
outer segments (Figs. 7, 11).When the inner
and outer segments are considered together
then the cell tapers more markedly (Figs. 3,
6, 7).
Within the foveola there are cones only
(Figs. 6, 7). Rods are present on the foveal
slopes (Fig. 5) and increase in number toward
the foveal periphery. At the foveal margin,
more rods than cones are present (Fig. 5).
Where rods and cones appear together, the
rod inner segment is much narrower than
the cone inner segment (Fig. 5).
On the surface of the outer segment there
can be seen imprints formed by the discs (or
saccules) they contain (Figs. 8,9,12).
When retinal detachment occurs during
preparation of tissue, some outer segments
break off. Most of the broken outer segments
366
B. BORWEIN
SEM OF MONKEY FOVEAL PHOTORECEF’TORS
remain embedded in the pigment epithelium
microvillous processes, but some microvillous processes of the pigment epithelium
break off and remain adhering closely to the
distal outer segment tip (Fig. 12).
DISCUSSION
The basic pattern of organization of photoreceptor cells is remarkably similar in all
classes of the vertebrate kingdom, but there
is nonetheless a wide range of variations in
these structures. SEM studies display these
A bbrewations
Bruch’s membrane
ciliary backbone
cone
choroid
ciliary connective
or cilium
calycal procesdes)
discs
external limiting
membrane
Henle fibers
Miiller cell
microvilli
outer segment
pigment
epithelium
rod
sclera
Fig. 1. A portion of the retina showing the foveal
slope and pit. The detached pigment epithelium lies free
below the outer segments. Note the thinning of the retina towards the foveal center. There is a pattern of radiating striations on the vitreal surface of the retina,
starting on the foveal slopes, but not affecting the floor
of the pit, the foveola. x70.
Fig. 2. A portion of the fundus viewed in vertical
section. There is an artefactual detachment in the foveal
region. The inner retinal layers are thinned. The choroid
(Ch) has a spongy appearance; the sclera (S)is fibrous.
Bruch’s membrane (B) appears as a narrow structureless
zone. ~ 1 7 0 .
Fig. 3. A view of the inner and outer segments of the
elongated foveal photoreceptors, seen in a vertical section through the retina. The cilia are aligned and appear
as a shadowy, wavy zone (Ci). The outer segments (0s)
bear nodules. Outer segments (arrow)can be seen on the
detached pigment epithelium (P),which is separated by
Bruch’s membrane from the spongy choroid (Ch). ~ 7 0 0 .
Fig. 4. The region of the foveal photoreceptor nuclei.
Empty nuclear nests (arrows), sharply angled Henle fibers (HI, the external limiting membrane (E), and the
ciliary zone (arrowhead) are clearly displayed. The microvilli of the Miiller cells, immediately scleral to the
external limiting membrane, are faintly discernible.
x 1,400.
367
variations in size, shape, and surface morphology very well (Borwein and Hollenberg,
1973; Breipohl et al., 1973; Dickson and Hollenberg, 1971; Hansson, 1970c; Lewis et al.,
1969; Pietzsch-Rohrschneider, 1976; Steinberg, 1973).
Photoreceptors, pigment epithelium, and
retina in general have been described by
SEM more extensively in vertebrates below
the Primates, but the sampling of the vertebrates i s rather limited. These studies fall
into several categories: (1)studies of retinal
and photoreceptor development of chick embryos (Breipohl et al., 1973, 1974a,b; Meller
and Tetzlaff, 1976; Olson, 1975, 1977, 1979)
and newborn albino rats (Galbavy and Olson,
1979; Garcia-Porrero and Ojeda, 1979); (2)
studies of adult mammalian retina-normal
and also in various experimental conditions-of albino rats (Hansson, 1970a-e;
Leuenberger, 1971; Puzzola et al., 1978; Puzzola and de Simone, 1979), rabbits (Aoki,
1974; Antal, 1977; Borwein et al., 1976,
1977a; Leuenberger, 1971; Miki et al., 1976;
Newton et al., 1980), mouse (Smith, 19731,
and cattle (Molday, 1976); (3) descriptions of
amphibian retinas of bullfrog (Steinberg,
19731, Necturus (mudpuppy) (Lewis et al.,
19691, and newt (Dickson and Hollenberg,
1971); (4)studies of dark- and light-adapted
retinas of fish (Ali and Wagner, 1976; Borwein and Hollenberg, 1973; Pietzch-Rohrschneider, 1976);( 5 ) studies partly or wholly
describing the pigment epithelium of albino
rats (Hansson, 1970a; Leuenberger, 1971;
Puzzola et al., 1978; Puzzola and de Simone,
19791, chickens (Breipohl et al., 1973), rabbit
(Borwein et al., 1977a; Leuenberger, 1971;
Miki et al., 19761, bullfkog (Steinberg, 19731,
and man (Goldbaum and Madden, 1982).
There have been only a few SEM studies of
primate photoreceptors. None is concerned
specifically with the fovea, a n area of particular interest since it subserves normal color
vision and photopic acuity. Knowledge of the
detailed morphology of the foveal photoreceptors is of major importance to a n understanding of their function.
Borwein et al. (1980) showed that both the
foveal and foveolar cone cells taper slightly
in their outer segments, and also when the
inner and outer segments are considered together. The dimensions were derived from
measurements taken of cross sections of foveal cone outer segments seen by TEM, a t
various levels, from their proximal bases to
their distal tips among the pigment epithe-
368
B. BORWEIN
SEM OF MONKEY FOVEAL PHOTORECEPTORS
369
They become particularly prominent, in both
rods and cones, as the junction of the inner
and outer segments is approached. It has
been suggested that the ridges are the outlines of the elongated inner segment mitochondria made apparent a s a result of tissue
shrinkage. This is very unlikely. In Primates, the mitochondria are frequently absent from the cone inner segment apex,
precisely the location where the ridges are
most pronounced. In TEM micrographs the
inner segment often shows a scalloped margin, but this is not always so. The ridges are
always seen in SEM preparations and regularly present the same appearance at the IS0s (inner segment-outer segment) junction.
The ridges may represent zones of a microtubular skeletal organization which may become more apparent and protrude on the
surface when the rest of the inner segment
shrinks during tissue processing. Engstrom (1963),in LM and TEM studies on fish,
saw that the calycal processes “do not really
begin at the outer tip of the ellipsoid but run
like mouldings along the surface of the entire
ellipsoid.” The ridges are within the inner
segments but the calycal processes, though
continuous with the longitudinal ridges, are
Fig. 5. A view of the foveal photoreceptors toward the
freestanding, and they surround the proximargin of the fovea, showing slender rod (R) and plump
cone (C) inner segments, bearing longitudinal surface
mal part of the outer segement in both rods
ridges. The narrowing of the inner segment toward the
and cones (Borwein et al., 1980; Brown et al.,
cilium is especially marked in the cones. Miiller cell
1963; Cohen, 1963).The calycal processes remicrovilli (MI surround the inner segments immediately
main attached to the inner segment if the
scleral to the external limiting membrane. ~ 2 , 0 0 0 .
outer segment breaks off, demonstrating
Fig. 6. A view of the central foveolar photoreceptors
their
continuity with the inner segments. In
showing the external limiting membrane (E), the shadmost animals, both the calycal processes and
owy line of the ciliary connectives (Ci), the nuclei 0,
the inner segment ridges are larger and more
and Henle fibers (H). Many cone outer segments can be
seen embedded among the microvillous processes of the
prominent in the cones than in the rods, as
detached pigment epithelium (P). The central cone outer
shown in this study.
and inner segments are in a straight line. The outer
By SEM it can be seen that calycal prosegments on either side of these tilt away from these
cesses surround the outer segment except for
central outer segments. ~ 4 0 0 .
the part around the ciliary backbone, as had
Fig. 7. The outer segments of the central cones seen
been seen in cross sections of monkey photoin Figure 6 are magnified to demonstrate their knobs
receptors viewed by TEM by Borwein et al.
and folds, their generally irregular outlines, and their
(1980), and by Reme and Young (1977) in
slight taper from their proximal to their most distal
ends. The external limiting membrane (E) and the ciliground squirrels. Calycal processes surround
ary region (Ci) are clearly displayed. X 1,400.
fish cones also but are not seen around its
associated accessory-outer segment (Borwein
Fig. 8. The foveal cones are seen at the region of the
and Hollenberg, 1973; Fig. 9, Braekevelt,
junction of the inner and outer segments. The calycal
processes (CP) arise from the longitudinal surface ridges
1975). This comparison prompts the queson the inner segments and become free-standing struction:
Is the accessory-outer segment homolotures which surround the proximal ends of the outer
gous
with the ciliary backbone? The SEM
segments, except for the area around the ciliary backalso shows clearly that only very short calybone. The calycal processes vary slightly in length and
are tapered. The discs (D) are clearly outlined on the
cal processes are associated with the cilium
surface of the outer segments. The cilium (Ci) has a very
area, and this was demonstrated also in TEM
uneven surface outline. A few very short calycal prostudies of cross sections of monkey photorecesses (arrowheads) and a ciliary backbone (CB) can be
ceptors (Borwein et al., 1980).
seen associated with the cilium. X 10,800.
lial cell processes; and of cone inner segments from near the ELM and also a t the
ellipsoid. It had become widely accepted that
foveolar and foveal cones are rodlike. While
a taper is very difficult to detect in longitudinal section, nevertheless a few workers had
previously suggested that such a taper exists
(for discussion on this see Borwein et al.,
1980). The SEM pictures confirm that there
is a slight taper in this very elongated cell.
The longitudinal surface ridges of the inner segments have been described in many
papers, both by LM and TEM (reviewed by
Borwein, 1981). The inner segment ridges
reported in this paper and by Borwein et al.
(1980) in monkey can also be seen in SEM
photomicrographs of the human cone cell
(Kuwabara, 19701, monkey cones (Smith and
Finke, 1972), mudpuppy cones (Lewis et al.,
19691, newt cones (Dickson and Hollenberg,
19711, and in teleost rods and even more
markedly so in the cones (Borwein and Hollenberg, 1973; Pietzsch-Rohrschneider, 1976).
These longitudinal ridges start in the myoid.
370
B. BORWEIN
SEM OF MONKEY FOVEAL PHOTORECEPTORS
Ueck et al. (1978) described and illustrated
by SEM “parallel oriented filamentous processes” (similar to calycal processes) surrounding the outer segment of pinealocytes
of a teleost fish, projecting from the apical
border of the inner segment and extending
to the tip of the rather squat outer segment,
and bearing small protrusions. This is the
only other reference to protrusions such as
we saw on the ridges near the calycal processes and the ciliary backbone (Figs. 9,lO).
The present study and prior studies demonstrate that primate outer segments of both
rod and cones are not always uniform but
present “bulbous swellings and other deformities” (Polyak, 1957). They are often displayed in light micrographs (e.g., p. 34,
Steinberg and Wood, 1979). Bonvein et al.
(197723) reported what appeared to be fused
human rod outer segments in cross sections,
by TEM. These findings were later reinterpreted by Marshall et al. (1979), who described “nodular excrescences” and “convolutions,’ in human rod outer segments, with
increasing incidence with age. These were
seen in both longitudinal and cross sections,
by LM and TEM. The nodular excrescences
or knobs are areas of intact discs which are
dislocated and rearranged within one outer
segment, while the convolutions are corrugations in the long axis so that curves are
formed by folds of ascending and descending
Fig. 9. Calycal processes (CP) can be seen a t the proximal ends of the outer segments. Outer segment discs
are apparent. Some of the outer segments are convoluted
or folded (arrowheads) on themselves. Others bear nodular excrescences. ~ 4 , 0 0 0 .
Fig. 10. A group of foveolar cones and one rod outer
segment (R). Note the small knoblike extensions from
the calycal processes, cilium, and inner segment surface
ridges (arrows). The ciliary backbone (CB) has no overlying calycal processes. The cilium (Ci) has a very irregular surface and with it are associated a few very short
calycal processes (CP). The long calycal processes show a
distinct taper. x 10,800.
Fig. 11. A group of foveolar photoreceptors several of
which show the outer segments folding on themselves in
their midregions (broad arrows). In the left-hand (upper)
corner there are two photoreceptors, the outer segments
of which have broken off, and calycal processes can be
seen extending beyond the fracture plane (thin arrow).
~2,700.
Fig. 12. Broken-off pigment epithelial cell microvillous processes are seen lying appressed to the distal tips
of foveal cones. The discs of the outer segments are
apparent. x 16,200.
371
portions of the outer segment. These convolutions and excrescences often contain normal-looking discs and were seen in otherwise
well-fixed material; their distribution was
discontinuous, and they appeared first in the
paramacula in the fourth decade (Marshall
et al., 1979). Borwein et al. (1980) reported
“knobs” and convolutions also in monkey
foveal cones, seen by TEM, and they are here
displayed by SEM, in both rods and cones.
The observations suggest that shedding and
phagocytosis may not be well synchronized
with disc renewal in older outer segments.
These convolutions and knobs appear to be
restricted to the midregion of the outer segment, beyond the calycal processes. The calycal processes may possibly function to keep
the outer segment shape and orientation intact close to the base where the new discs are
constantly being formed.
SEM is a n ideal tool for investigations of
the calycal processes, the Muller cell microvilli, and the overall cell shape because the
full lengths and widths can be seen simultaneously. This SEM study has shown with
special clarity several features of the calycal
processes: That they taper, except for those
two or three which are very short and stublike in the immediate vicinity of the ciliary
connective; that there are no calycal processes around the ciliary backbone; that the
calycal processes seem to be continuous with
the longitudinal ridges of the inner segment;
that if the outer segment breaks off near the
inner segment-outer segment junction the
calycal processes remain intact and attached
to the inner segment. The study also shows
the slight taper of the foveal cone outer segments, and it displays the convolutions and
bulges of the outer segments which were
shown by Marshall et al. (1979) to increase
in frequency with age. While TEM yields
rich information on the morphology of the
cell interior and cellular associations, SEM
is particularly valuable as an adjunct to TEM
studies, in its emphasis on cell shape and
surface features.
ACKNOWLEDGMENTS
I wish to thank Mrs. Artee Karkhanis and
Mr. Stephen Smith for their excellent technical assistance.
This research was supported by the U S .
Army Medical Research and Development
Command (No. DAMD 17-80-G-9466)and the
Medical Research Council of Canada. The
views and opinions herein do not necessarily
372
B. BORWEIN
reflect the positions or decisions of the Army
and no official endorsement should be inferred.
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