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Fine structure of photoreceptors in the owl monkey.

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Fine Structure of Photoreceptors in the
Owl Monkey’
RAYMOND G. MURRAY, ARTHUR E. JONES AND ASSIA MURRAY
Department of Anatomy and Physiology and the Division of Optometry
Physiological Optics, Indiana University, Bloomington, Indiana 47401
ABSTRACT
The owl monkey (Aotes trivirgatus) differs from most primates
in being nocturnal in habit and having primarily scotopic vision. Photoreceptor
cells of the retina of this species were studied with the electron microscope and
compared with corresponding cells of other primates. N o striking qualitative
differences were noted. Most of the receptors are typical rods, but approximately
5% are cones, based on the following features: shorter, tapering outer segments,
discs with smooth rather than scalloped margins and with uniformly narrow internal spaces, the membranes of which in some cases are continuous with the
plasma membrane; broad inner segments with numerous mitochondria; nuclei
that lie immediately against the outer junctional zone (outer limiting membrane) with relatively thick inner fibers leading to large pedicles in the floor of
which are numerous typical “synaptic triads.” One relatively unusual feature
of the rods is the prominence of the striated rootlets associated with the basal
bodies of the cilium-like connecting pieces. An apparently intimate relation of
the rootlets to investing mitochondria, especially to their tubular internal cristae,
is discussed with regard to the possibility of a function for the rootlet other than
static anchoring of the cilium.
Investigation of the primate retina has
quite naturally centered on the human
(Polyak, ’41), and the study of the fine
structure has had a similar emphasis
(Smelser, ’61). The basic features of the
fine structure of the human retina are well
established (Missotten, ’65). The retinas of
other primates, of which the most extensively studied h a s been Macaca mulatta,
appear to have a quite similar fine structure. The electron microscope has provided
a level of resolution which permits accurate visualization of the complex ramifications and connections of the retinal neurons, and by which a “wiring diagram” is
beginning to take shape (Dowling and
Boycott, ’65; Dowling and Boycott, ’69;
Sjostrand, ’69). Analysis of the functional
significance of the various elements might
be aided by comparative study of other
primates with distinctly different behavioral characteristics. The owl monkey
(Aotes trivirgatus) is nocturnal in habit
and has primarily scotopic vision. Its retina
was originally described as possessing only
rod receptors (Schultze, 1872). However,
ANAT. REC.. 175: 673-696.
Jones and Jacobs (’63) presented physiologic evidence of a duplex retina in this
species, which was subsequently confirmed
by the physiological and light microscopic
studies of Hamasaki (’67). Cone-like receptors have also been identified in electron micrographs, (de Olivera and Ripps,
’68) but without extensive documentation
of the features that characterize this
second type of receptor. The present report
describes the fine structure of the photoreceptors of the owl monkey.
METHODS
Five light adapted male owl monkeys
(Aotes trivirgatus) were used in this study.
Under nembutal anesthesia the animals
were either perfused through the left heart
with 4% paraformaldehyde ( 3 animals)
or the eyes excised and placed directly in
fixative, one eye in 1% OsOc and the other
Received Nov. 10, ’71. Accepted Nov. 27, ’72.
1This research was supported in part by contract
DADA17-70-C-0010 from the U. S. Army Medical Research and Development Command and in part by
grant PHS N S 07472 from the NatiAnal Institutes of
Health, United States Public Health Service.
673
674
R. G. MURRAY, A. E. JONES AND A. MURRAY
A. Rods
in 6% glutaraldehyde ( 2 animals). The
perfusing fluid was warmed to 40°C, but
Our description will proceed in general
all other fixing and dehydrating procedures from scleral to vitreal portions. The outer
were carried out in an ice bath. In each segment has a diameter of approximately
case the aldehyde or OsO, was buffered 1 and a length of approximately 20 p ,
to pH 7.2-7.4 with phosphate buffer These dimensions are relatively uniform
(Millonig, ’61) and the excised eyes were over much of the retina. The tips of these
opened by removing the anterior part, in- segments are enveloped by processes of the
cluding the lens, with a razor blade cut. pigment epithelial cells and various stages
Whether perfused or not, the eyes after be- of what we presume to be detachment and
ing opened stood for one-half to one hour disintegration of portions of the outer segin the aldehyde solution or in OsO,. After a ments within the pigment epithelium are
brief rinse in buffer, pieces of retina were evident (fig. 2 ) . Such a process of rod
excised with a razor blade, immersed for outer segment removal has been well docua total time of one and one-half to two mented for other primates (Young, ’71).
hours in 1% OsO, i n Millonig buffer, de- In longitudinal sections the outer segment
hydrated in a graded series of acetones is seen to be filled with a stack of discs,
beginning with 6596, embedded in Epon the paired membranes of which are inde812 or Araldite 502, and sectioned with a pendent of the plasma membrane, In secdiamond knife. The sections were stained tions perpendicular to the long axis of the
rods those discs present a scalloped margin
in saturated aquaeous solutions of uranyl (fig. 3 ) . The outer segment connects with
acetate and examined in a Hitachi HU- the inner by a slender stalk (fig. 4). At
11 A electron microscope. No significant the root of the stalk are two centrioles,
variations in appearance were correlated one of which is a basal body which gives
with the different processing procedures origin to a cilium-like structure with nine
employed.
tubular elements (fig. 3 ) ascending in the
Counts of receptor types were made i n connecting piece between inner and outer
low magnification electron micrographs of segments of the rod. These processes exsections cut normal to the outer junctional tend along one side of the base of the outer
zone (OJZ).* The areas selected were those segments, one or more of them lying
which passed through the transition zone closely adjacent to the rod sacs. Transverse
between the inner and outer segments of sections just below the outer segment also
the rods. In such sections rod inner or show that the stalk is surrounded by five
outer segments are easily distinguished regularly spaced microvillous projections
from the cone outer segments which are from the inner segment which give the
found at this level of the retina. Both entire profile here the appearance of a
peripheral and central areas of two mon- five pointed star (fig. 3b).
The question of a n additional broader
keys were studied in this manner, employing 25 micrographs and counting approxi- connection between inner and outer segments was given special attention in view
mately 2000 receptors.
of a recent report by Richardson (’69) that
For light microscopy, 1 or 3 sections such broad connections are typical in
were mounted unstained on glass slides mammalian retinae. We have never seen
and examined with dark contrast phase in our material a convincing demonstraoptics.
tion of continuity of cytoplasm such as
Richardson
illustrated for rat and guinea
RESULTS AND INTERPRETATIONS
pig retinae. We do occasionally see irreguA survey view of the retina as seen larly shaped rods with direct continuity of
by phase microscopy is presented in the type described by Tokuyasu and
figure 1. The majority of receptors appear Yamada (’60) and agree with these auto be rods, but a small fraction differ sig- thors that these represent abnormal forms.
nificantly. We shall first describe the rods,
2 We have employed the more accurately descriptive
and then the second receptor type, which term “outer junctional zone” rather than “outer limiting membrane” in keeping with the suggestion of
we believe to be cones.
Hendrickson ( ’ 6 6 ) .
PHOTORECEPTORS OF OWL MONKEY
It is our opinion, therefore, that in Aotes
trivirgatus the connection is through the
slender cilium stalk alone, except perhaps
in isolated unusual cases.
A second centriole at right angles to the
basal body is usually present. A striated
rootlet takes origin from the region of the
two centrioles (fig. 4). It relates most intimately to the basal body, but a direct connection can seldom be demonstrated. The
rootlet corresponds to that seen in the rods
of higher primates (Bloom and Fawcett,
'68), being composed of a bundle of fibrils
50 to 70 A in diameter with cross bands
that show a primary period of 800 to 900
A and secondary bands, varying in number
and spacing, between the primary bands.
The bundle does not have an independent
limiting membrane, but is confined
throughout most of the inner segment by
closely adherent mitochondria (fig. 4 ) and
at lower levels large, empty cisternae of
endoplasmic reticulum lie closely adherent
to it. The rootlets are unusually prominent
in this species, extending through the outer
junctional zone (OJZ) to the nuclear level.
In some cases the cross striation can be
seen to extend beyond the edges of the rootlet, as if to provide anchoring contacts
(fig. 5 ) . In addition, the major cross band
shows a consistent polarity, having a
sharp distal and less well defined proximal
border.
The largely tubular cristae of mitochondria adjacent to striated rootlets often
appear to have a special relation to the
dark band of the major periodicity. The extent of this relationship was roughly evaluated in a group of micrographs picked
essentially at random from the collection.
All instances where rootlets were present
in sufficient detail so that the relationship
with tubules could be clearly visualized,
were evaluated (38 cases). In 24 cases at
least 65% of contacts were with dark
bands. Of the remainder, eight favored the
dark band by a lesser percentage, five had
approximately equal contacts with dark or
light bands and only in one case were the
light intervals contacted more often. Although the relative widths of the bands
varied, the light intervals were always at
least twice the width (fig. 4, 5 , 6, 1 1 ) of
the dense strip we have called the major
675
period band. If contacts were random they
should be more frequent with the broader
zone, while the contrary appears to be the
case. In many instances the registry of
tubules and dark bands is quite striking.
Other elements present in the inner segment are microtubules, oriented primarily
in the long axis of the rod, a few granules
which may be glycogen, scattered ribosomes, and cisternae of the endoplasmic
reticulum. Rough-surfaced cisternae are
prominent just above the OJZ, but elsewhere the cisternae are smooth-surfaced.
A group of Golgi membranes and vesicles
is also present above the OJZ. Uga, et al.
('70) recently demonstrated an additional
fine fibrillar element in human rod inner
segments. They were widely distributed but
most prominent near the centrioles where
they formed regular aggregations with a
wavy pattern. We have not seen such
fibrils, but areas of amorphous to vaguely
granular material between the other cytoplasmic constituents may represent a
poorly preserved fibrillar component.
In the central area of the retina the
outer nuclear zone may contain as many
as six to eight layers of nuclei. The vast
majority are presumably rod nuclei, but, in
fact, they are all so similar in appearance
that it is not possible accurately to classify
the receptors on the appearance of their
nuclei alone. The cytoplasm of most rods
narrows abruptly as i t passes the OJZ, to
form a uniform process about 0.5
in
diameter filled with microtubules (fig. 7).
None of the other cytoplasmic elements
mentioned above was observed here. This
description also applies to the inner fibers
of those rods with nuclei far out in the
layer, as they take origin from the vitreal
end of the perikaryon and proceed toward
the outer plexiform layer. In this layer the
inner fibers expand into an ending with
basic features corresponding to the rod
spherule (fig. 8 ) as described for other
primate species (Cohen, '63; Yamada et al.,
'58). Those rods which have their nuclei
close to the outer plexiform layer are without an inner fiber. The synaptic complex,
with the invaginated processes of other
neurons and the typical dense synaptic ribbon or disc, are present in the cytoplasm
close to the nucleus.
676
R. G . MURRAY, A. E. JONES AND A. MURRAY
B.
The second type of receptor
sections examined by phase
In 1-3
contrast microscopy (fig. 1 ) a few outer
segments are distinctly shorter than the
majority and originate well below (vitread)
the general level of outer segments. The
associated inner segments are broader and
paler than the rest, but otherwise not strikingly different. They can usually be related
to nuclei which lie just beneath the OJZ.
These features suggest that these are cone
receptors, and we shall refer to them
henceforth as cones, on the basis of morphological evidence now to be detailed. In
our preliminary counts of the relative number of cones we found values from 3 to 6%
which did not vary consistently in relation
to central or peripheral locations. A similar relative uniformity was reported by
Hamasaki (’67) except that he designated
all the receptors in the area centralis as tall
rods. Some of our sections contain parts
of the area centralis but do not constitute
an exhaustive survey of this entire region.
We found no area lacking cones, although
it is possible that a very small area of this
character might have been missed by this
procedure.
With the electron microscope the cones
are most easily recognized by their outer
segments, which take origin much more
vitread than do those of the rods (fig. 9).
Based on the description of rods above, the
cones show essentially all the features
usually cited (Cohen, ’ 6 3 ) to distinguish
them from the rods. The inner segment is
broader and more heavily populated with
mitochondria. In sections normal to the
OJZ and passing through the mitochondral
zone of the inner segments, the number of
mitochondral profiles in rods ranges from
10 to 20 while in cones the range is from
20 to 50. The difference between the two
receptors in this respect is thus not nearly
SO marked as the ratio of 1:20 reported for
the human by Yamada et al. (’58). The
outer segment tapers only slightly from
the base, but the broader inner segment
gives the receptor a slender conical shape.
The tips of the outer segments are surrounded by cytoplasmic processes of pigment cells containing pigment granules.
In horizontal sections (parallel to the
OJZ) the outer segments of the cones are
typically isolated from surrounding rods as
they narrow toward the tip (fig. 10). The
outline of their discs is smooth rather than
scalloped.
The union of inner and outer segments,
is much the same as seen in rods where
outer and inner segments are joined only
by a narrow bridge (fig. 11). Above the
contact zone the double-membrane discs
begin, but all are not true discs, independent of the surface. If the pairs of membranes constituting a “disc” are traced to
the surface, in some instances the membranes separate and become continuous,
in opposite directions, with the plasma
membrane. This condition exists frequently
near the contact zone, but becomes less
frequent toward the sclera. Rod and cone
membranes differ also in the space separating the pairs of membranes, for in the
cones it is narrow and uniform while in
the rods more irregular and generally
wider. These features are illustrated in
figure 12 which compares the bases of
outer segments of a rhesus cone with those
of a rod and cone of owl monkey. These
features are now recognized as characteristic differences between primate rods and
cones (Bloom and Fawcett, ’68).
There are, in cones, a basal body, a
second centriole and a striated rootlet, the
latter being not so well developed, nor extending so far vitread, as in the rods. The
nucleus lies just below the OJZ and in
rare cases may protrude into it, but except
for its position, it is not strikingly different,
under our conditions of preparation, from
the surrounding rod nuclei. The inner fiber
is broader than that of rods and contains
occasional mitochondria in addition to the
dense packing of microtubules. It expands
at the vitreal side of the outer plexiform
layer into a sac which is much larger than
the rod spherules (fig. 8 ) and resembles,
in all basic respects, the cone pedicle of
other primates (Missotten, ’65). Perhaps
most significant is the fact that there are
many “triad-type” synaptic contacts in
these pedicles, while the rod spherules contain only one group of invaginating processes (fig. 8).
C . Other considerations
In all the eyes examined, there was a
central area about 6-8 mm temporal to the
entrance of the optic nerve, and about 4
PHOTORECEPTORS OF O W L MONKEY
mm in diameter, which could be distinguished in the unfixed, or aldehyde-fixed
condition. After fixation in OsO, this central area could no longer be distinguished.
Portions of this central area were, therefore, singled out for specific study before
OsO, fixation. Both phase contrast and electron microscopy revealed blood vessels in
all of these specimens as far out as the
outer plexiform layer, and showed the relative numbers of receptor types to be similar
whether the sample was from the margin
or nearer the center of this area. In none
was there a particularly dense packing of
receptor elements, as in the human fovea.
It is conceivable that a very small, highly
specialized area could have been missed
by this procedure, but it seems more likely,
as reported by de Oliveira and Ripps ('68),
that no avascular area exists in this
species.
Since Uga et al. ('70) have recently reported junctions between the inner segments of human receptor cells, we have
looked for this condition in our material.
Although these elements were frequently in
contact, no junctional structures or cytoplasmic continuities were observed.
DISCUSSION
The fine structure of the retina of Aotes
trivirgatus displays no strikingly unique
features. There exists a receptor type
which corresponds to human cones, although they are relatively few in number
and not heavily concentrated in any area.
Identification of cones cannot be made on
quick inspection but requires careful individual analysis (fig. 1 1 ) . This is consistent with the delay in their positive
identification in this species. Since the
number and concentration of cones is correlated with visual acuity in the human
and other species, the relative lack of this
element in owl monkey and the prominence of rods is consistent with their nocturnal habits and low visual acuity. It is
perhaps surprising, in fact, that a nocturnal animal would have so extensive a
cone system. It is now known, however,
that species of bats which have extremely
limited visual sense also have typical conetype receptors in their retinae (Chase,
'70). This suggests that cones have a
fundamental part to play in any type of
677
visual response rather than being considered a special type of receptor for special
purposes. Further studies of the visual discriminatory parameters in owl monkey,
correlated with analyses of the pattern of
connections at the level of the first synapses and beyond, might provide new insights into retinal mechanisms in general.
The cross-banded rootlet which extends
downward from the cilium, although not a
prominent feature of human retinae
(Cohen, '63), appears to be especially well
developed in the owl monkey. Certain features relating to it deserve special comment. Immediately below its origin the
rootlet is tightly invested by a nearly complete sheath of mitochondria which is replaced by closely adherent cisternae of endoplasmic reticulum at lower levels. The
cristae of these mitochondria are frequently in register with the dark bands of
the cross striation, suggesting that energy
transfer may be occurring at these points.
Olsson ('62) described a similar intimate
relation between mitochondria and rootlets
associated with the cilia of Amphioxus
lanceolotus. He also noted a pronounced relationship between the dark periods of the
rootlet striation and the mitochondria1
cristae, and speculated that some metabolic relationship might exist. Chase ('72)
noted a similar relationship in the retinae
of several species of bats. In our material,
the close proximity of the rootlets to the
endoplasmic reticulum adds weight to the
possibility that the rootlets may be involved
in some active process. Sjostrand ('53)
suggested a possible conductile function,
and Orzalesi and Bairati ('64) seemed to
favor a kinetic function for some situations. On the other hand, there appear to
be many cases where a more static anchoring function is indicated (Fawcett, '58;
Gibbons, '61; Olsson, '62). In our case, the
suggestion that the cross striations extend
laterally to make contact with other cytoplasmic material could indicate a static
function, or relate to a necessity to attach
to the cell skeleton in order to perform a
kinetic function. In any case, the prominence of the rootlet in the owl monkey
retinal receptors provides an opportunity
to study their functional significance. The
possibility of changes in form or periodicity
of the cross bands, under conditions of
678
R. G. MURRAY, A. E. JONES AND A. MURRAY
light and dark adaptation, should be
explored.
LITERATURE CITED
Bloom, W., and D. W. Fawcett 1968 A Textbook of Histology. W. B. Saunders Co., Philadelphia, pp. 776-811.
Chase, J. 1970 Variation of retinal structure
in diverse species of echolating bats. The
Physiologist, 13: 166.
1972 The role of vision i n echolocating
bats. Doctoral dissertation. Indiana University,
Bloomington, Indiana.
Cohen, A. I. 1963 Vertebrate retinal cells and
their organization. Biol. Rev., 38: 427459.
de Oliveira, L. F., and H. Ripps 1968 The “area
centralis” of the owl monkey. Vis. Res., 8 :
223-228.
Dowling, J. E., and B. B. Boycott 1965 Neural
connections of the retina: structure of the inner
plexiform layer. Cold Spring Harb. Symp., 30:
393-402.
1969 Retinal ganglion cells: a correlation of anatomical and physiological approaches. In: The Retina: Morphology, Function
and Clinical Characteristics. B. R. Straatsma,
M. 0. Hall, R. A. Allen and F. Cresitelli, eds.
University of California Press, pp. 145-161.
Fawcett, D. W. 1958 Structural specialization
of the cell surface. In: Frontiers in Cytology.
S. L. Palay, ed. Yale University Press, New
Haven, pp. 19-41.
Gibbons, I. R. 1961 The relationship between
the fine structure and direction of beat i n gill
cilia of a lamellibranch mollusc. J. Biophysic.
Biocl-em. Cytol., 11 : 179-205.
Hamasaki, D. 1. 1967 An anatomical and electrophysiological study of the retina of the owl
monkey, Aotes triuzrgatus. J. Comp. Neur., 130:
163-173.
Hendrickson, A. 1966 Landolt’s club in the
amphibian retina: a Golgi and electron microscope study. Invest. Ophtholmol., 5: 484497.
Jones, A. E., and G. H. Jacobs 1963 Electroretinographic luminosity functions of Aotes
monkey. Amer. J. Physiol., 204: 47-50.
Millonig, G. 1961 Advantages of a phosphate
buffer for OsOl solutions in fixation. J. Appl.
Phys., 32: 1637.
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Missotten, L. 1965 The Ultrastructure of the
Human Retina. Editions Arsica, Brussels,
Belgium.
Olsson, R. 1962 The relation between ciliary
rootlets and other cell structures. J. Cell. Biol.,
15: 596-599.
Orzalesi, N., and A. Bairati 1964 Filamentous
structures in the inner segment of human
retinal rods. J. Cell. Biol., 20: 509-514.
Polyak, S. L. 1941 The Retina. The University
of Chicago Press, Chicago.
Richardson, T. M. 1969 Cytoplasmic and
ciliary connections between the inner and outer
segments of mammalian visual receptors. Vis.
Res., 9: 727-731.
Schultze, M. 1872 ttber den Bau der Netzhaut
von Nyctipithecus felinus. Sitzunberg. d.
Niederrhein. Gesells. f. Natur-u. Heilkund. Cf.
Verhandl. d. Naturhist. Ver. d. Preuss. Rheinl.
u. Westph., 29: 158.
Smelser, G. K. ( e d ) 1961 The Structure of the
Eye. Academic Press: New York and London.
Sjostrand, F. J. 1953 The ultrastructure of the
inner segments of the retinal rods of the
guinea pig as revealed by electron microscopy.
J. Cell. Comp. Physiol., 42: 45-70.
1969 The outer plexiform layer and the
neural organization of the retina. In: The
Retina: Morphology, Function and Clinical
Characteristics. B. R. Straatsma, M. 0. Hall,
R. A. Allen and F. Cresitelli, eds. University of
California Press, pp. 63-100.
Tokuyasu, K., and E. Yamada 1960 The fine
structure of the retina: Abnormal retinal rods
and their morphogenesis. J. Biophys. Biochem.
Cytol., 7: 187-190.
Uga, S., F. Nakao, M. Mimura and H. Ikui 1970
Some new findings on the fine structure of the
human photoreceptor cells. J. Electron Microscopy, 19: 71-84.
Yamada, E., K. Tokuyasu and S. Iwaki 1958
The fine structure of the retina studied with the
electron microscope. 111 Human retina.
J. Kurume Med. Assn., 21: 1979-2027.
Young, R. W. 1971 Shedding of discs from
rod outer segments in the rhesus monkey.
J. Ultrastr. Res., 34: 190-203.
PLATES
All micrographs (with 1 indicated exception) are of owl monkey (Aotes
trivirgatus) retina, fixed either by perfusion in buffered glutaraldehyde
followed by 0 ~ 0 4 , sectioned in Epon and stained with uranyl acetate
(POA-E-UA), or fixed directly in OsO,, sectioned in Araldite and stained
with uranyl acetate (0-A-UA) as indicated.
PLATE 1
EXPLANATION OF FIGURE
1 Survey phase micrograph ( l a ) of the entire width of a peripheral
region of the retina. The vast majority of the inner segments of the
receptors are slender rods. Two are shorter and broader (arrows)
associated with outer segments that extend below the others, and
with nuclei immediately vitread from the outer junctional zone (OJZ).
Many rod spherules ( R S ) and several larger endings suggesting cone
pedicles ( C P ) are seen in the other plexiform layer (OPL). In 1b the
region of the receptor cells has been enlarged to show a cone ( C )
and one of the pedicles (CP) in greater detail. Mitochondria can be
visualized in both spherules and uedicles. and several invaeinatine
synaptic contacts are seen in the-floor of the pedicle. 0-A-%A (a:
X 1200; ( b ) x 2500.
PHOTORECEPTORS OF O W L MONKEY
PLATE 1
R. G . Murray, A. E. Jones and A. Murray
681
PLATE 2
EXPLANATION OF FIGURES
2
Tips of outer segments (0s) in contact with pigment epithelium
(PE). At arrows are two bodies that appear to be detached portions
of outer segments included in the cytoplasm of the pigment epithelium. POA-E-UA x 19,000.
3 A section perpendicular to the long axis of the rods. In ( a ) the section passes through the tip of an inner segment (IS) and the connecting piece. In ( b ) another connecting piece has been cut at a little
higher level, and is surrounded by five microvillus extensions of the
inner segment. The scalloped margins of rod discs are evident in the
profiles of outer segments also present. 0-A-UA x 43,000.
PHOTORECEPTORS OF O W L MONKEY
R. G . Murray, A. E. Jones and A. Murray
PLATE 2
683
PLATE 3
EXPLANATION OF FIGURE
4 Region of junction of rod inner (IS) and outer ( 0 s ) segments. The
two central rods each show a pair of centrioles, one of which is the
basal body of a cilium-like connecting piece. Striated rootlets extend
downward from the basal body. One of these ( S R ) is intimately surrounded by mitochondria ( M ) . The other centriole of the pair is
unrelated either to the cilium or the rootlet. Irregular saccular profiles are present in the base of the outer segments( arrows) and in
one case ( * ) appear to be related to one of the small ciliary tubules.
The tubules of this connecting piece appear faintly cross-striated
with a period approximating that of the spacing of rod discs.
0-A-UA x 27,000.
684
PHOTORECEPTORS OF O W L MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE 3
685
PLATE 4
EXPLANATION OF FIGURES
5
Detail of striated rootlet in a rod inner segment. At arows the
transverse bands seem to continue into the adjacent cytoplasm. A
cone outer segment (COS) is at the left. POA-E-UA x 100,000.
6 Striated rootlet in rod inner segment closely invested by mitochondria.
Many of the tubular cristae are related (arrows) to the major bands.
POA-E-UA x 60,000.
7 Region just vitread from the OJZ. Note nuclei of receptor cells ( N )
and the narrowed continuation of a rod ( R ) filled with microtubules.
0-A-UA
686
x
19,000.
PHOTORECEPTORS OF OWL MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE
4
687
PLATE 5
EXPLANATION OF FIGURE
8
Junction of outer nuclear and outer reticular layers. Numerous
rod spherules ( R S ) and one cone pedicle (CP) are present. 0-A-UA x
11,500.
688
PHOTORECEPTORS OF OWL MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE 5
689
PLATE 6
EXPLANATION O F FIGURES
9 Junction between inner and outer segments of a rod (R) and a cone
( C ) . The cone is broader, with more numerous mitochondria in the
inner segment. POA-E-UA
x 22,000.
10 Transverse section through one cone ( C ) and several rod ( R ) outer
segments, near the upper end of the cone. Note the smooth outline
and relative isolation of the cone, and the scalIoped outline of the
rods. 0-A-UA x 22,000.
690
PHOTORECEPTORS OF OWL MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE 6
691
PLATE 7
EXPLANATION O F FIGURE
11 Junction of inner ( I S ) and outer ( 0 s ) segments of a cone. Although
from this micrograph it may appear to be a rod, adjacent micrographs
of the same cell enable positive identification as a cone. There is
no cytoplasmic continuity except through the connecting piece (CP).
A basal body and poorly defined striated rootlet are present. In the
base of the outer segment sacs of EPR presumably represent early
stages of disc formation. Continuities of disc membranes with the
plasma membrane are not demonstrated, probably due to the plane
of section. 0-A-UZ x 32,000.
692
PHOTORECEPTORS OF OWL MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE 7
693
PLATE 8
EXPLANATION OF FIGURE
12 Comparison of outer segments of a cone of rhesus ( A ) , a cone of
owl monkey ( B ) , and a rod of owl monkey ( C ) . Continuities of disc
membranes with t h e plasma membrane (arrows) are numerous in
( A ) , less common i n ( B ) , and not seen i n (C). Note also the greater
irregularity of the rod discs with regard to orientation as well as
intra- and interdisc spaces. PAO-E-UA x 60,000.
694
PHOTORECEPTORS OF OWL MONKEY
R. G. Murray, A. E. Jones and A. Murray
PLATE 8
695
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