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Morphological and Morphometric Study of the Pecten Oculi in the Budgerigar (Melopsittacus undulatus).

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THE ANATOMICAL RECORD 295:540–550 (2012)
Morphological and Morphometric Study
of the Pecten Oculi in the Budgerigar
(Melopsittacus undulatus)
ANTONIO MICALI,1 ANTONINA PISANI,1 CLAUDIA VENTRICI,1
DOMENICO PUZZOLO,1* ANNA MARIA ROSZKOWSKA,2
ROSARIA SPINELLA,2 AND PASQUALE ARAGONA2
1
Department of Biomorphology and Biotechnologies, Section of Histology and Embryology,
University of Messina, Policlinico Universitario, Via Consolare Valeria 1, I-98125,
Messina, Italy
2
Department of Surgical Specialties, Section of Ophthalmology, University of Messina,
Policlinico Universitario, Via Consolare Valeria 1, I-98125, Messina, Italy
ABSTRACT
The pecten oculi is a highly vascular and pigmented organ placed in
the vitreous body of the avian eye. As no data are currently available on
the morphological organization of the pecten in the Psittaciformes, the
pecten oculi of the budgerigar (Melopsittacus undulatus) was studied.
The eyes from adult male budgerigars were examined by light, transmission, and scanning electron microscopy and a morphometric study on
both light and transmission electron microscopy specimens was also
performed in the different parts of the organ. In the budgerigar, the type
of the pecten oculi was pleated. Its basal part had a cranio-caudal and
postero-anterior course; its body consisted of 10–12-folds joined apically
by a densely pigmented bridge. The pecten showed many capillaries,
whose wall was thick and formed by pericytes and endothelial cells.
These latter had a large number of microfolds, rectilinear on their luminal surface and tortuous on their abluminal surface. Interstitial pigment
cells were placed among the capillaries, filled with melanin granules and
showed many cytoplasmic processes. The morphometric analysis demonstrated significant differences among the three parts of the organ relative
to the length of the endothelial processes and to the number and size of
the pigment granules. The morphological and morphometric analysis
showed that the bridge of the budgerigar, different from the other birds,
had a large number of capillaries, so that this part of the organ could
also play a trophic role for the retina in addition to the choriocapillaris.
C 2012 Wiley Periodicals, Inc.
Anat Rec, 295:540–550, 2012. V
Key words: pecten oculi; capillaries; endothelial cells; pigment
cells; morphometry; Melopsittacus undulatus
INTRODUCTION
The pecten oculi is a highly vascular and heavily pigmented structure, placed in the vitreous chamber, along
the course of the fetal fissure of the eye of all examined
avians. It is considered as an indirect retinal trophic system (Michaelson, 1954), as it supplements via the vitreous humor the choriocapillaris, the only constant retinal
direct system observed in vertebrates (Puzzolo, 1994).
The pecten can show three different morphological
patterns. The conical type, observed only in the paleognath kiwi (Rochon-Duvigneaud, 1943; Meyer, 1977),
C 2012 WILEY PERIODICALS, INC.
V
*Correspondence to: Domenico Puzzolo, M.D., Department of
Biomorphology and Biotechnologies, University of Messina,
Torre Biologica—Policlinico Universitario, Via Consolare Valeria
1, I-98125, Messina, Italy. Fax: þ39 90 692449.
E-mail: nico.puzzolo@unime.it
Received 24 September 2011; Accepted 4 January 2012
DOI 10.1002/ar.22421
Published online 20 January 2012 in Wiley Online Library
(wileyonlinelibrary.com).
THE PECTEN OCULI OF THE PARROT
resembles the papillary cone of the lacertilia (Micali
et al., 1988) and shows a cylindrical shape. The vaned
type, typical of other paleognaths, such as the ostrich
(Kiama et al., 2006) and the rheas (Meyer, 1977), is
formed by a central pillar, around which many vertical
and thin lamellae are placed. The pleated type, found in
a large number of neognaths, is well studied either during its development (Puzzolo et al., 1980; Parducci et al.,
1987; Uehara et al., 1990; Liebner et al., 1997) or in the
adult (Fischlschweiger and O’Rahilly, 1966; Raviola and
Raviola, 1967; Fielding, 1972; Jasinski, 1973; Dieterich
et al., 1973; Bawa and YashRoy, 1974; Dieterich and
Dieterich, 1974; Braekevelt, 1984, 1988, 1994, 1998;
Puzzolo et al., 1985a; Kiama et al., 1994, 1997, 1998;
Braekevelt and Richardson, 1996; Smith et al., 1996;
Scala et al., 2002; Rahman et al., 2010; Gültiken et al.,
2011). The pleated type is composed of three different
parts: the base, adjacent to the neuroretina, the folds,
arranged like an inverted fan, and the bridge, running
like a handrail along the vitreous margin of the organ.
Structural and ultrastructural studies have demonstrated the constant presence of a superficial limiting
membrane covering the entire pecten (Braekevelt, 1998),
of hyalocytes (Uehara et al., 1996), of a large number of
interstitial pigment cells (Dieterich and Dieterich, 1974),
and of many capillaries; these latter are surrounded by
a thick basement membrane (Braekevelt, 1984; Corona
et al., 2004) and formed by endothelial cells with long
microfolds on both luminal and abluminal surfaces
(Braekevelt, 1988; Scala et al., 2002) and by some abluminal pericytes (Raviola and Raviola, 1967; Rahman
et al., 2010).
The size and the shape of the pecten and the number
of its folds showed peculiar variations (Braekevelt,
1988), which were considered independent to the eye
size but were rather related to the environmental lighting (Bawa and YashRoy, 1972) and to the activity of the
bird (Kiama et al., 2006).
No data are currently available on the fine morphology of the pecten in the order of Psittaciformes, such as
the budgerigar Melopsittacus undulatus (Shaw, 1805), a
largely available and easily handling species. In this
work, we provide morphological and morphometric data
on the pecten oculi of this bird to demonstrate its structural and ultrastructural organization and to present
the first morphometric data on the blood vessels and on
the pigment cells in the different parts of the organ.
MATERIALS AND METHODS
The work was carried out in the Department of
Biomorphology and Biotechnologies of the University of
Messina, Italy, during the 2009 spring and fall seasons.
Animal treatment and experimentation were carried out
in accordance with NIH Guidelines for the Care and Use
of Laboratory Animals. Four adult male light-adapted
budgerigars M. undulatus (Shaw, 1805) (Psittaciformes,
Psittacinae) were provided by a local dealer. The animals
were acclimated for at least two days before the euthanasia to recover from the stress induced by transportation and the changes in environment. They were housed
in individual cages under a L:D regimen of 12 hrs each
with water and diet ad libitum. The budgerigars
were euthanized by CO2 inhalation followed by cervical
541
dislocation and the eyes were immediately enucleated
and processed for light and electron microscopy.
Light Microscopy
Four right eyeballs were cut with a razor blade along
the equator and the posterior parts were fixed in 2.5%
glutaraldehyde in 0.2 M phosphate buffer (pH 7.4) at
þ4 C for 2 hrs, washed with 0.2 M phosphate buffer (pH
7.4), and postfixed in 1% OsO4 in 0.2 M phosphate buffer
(pH 7.4) at þ4 C for 1 hr. After dehydration in graded
ethanol and acetone, the pectineal regions were isolated
and flat embedded in Durcupan. Semithin sections
(1 lm) were cut with a LKB Ultrotome V ultramicrotome, stained with 1% toluidine blue in 1% borax and
1% pironine (Holstein and Wulfhekel, 1971) and viewed
and photographed with a Zeiss Primo Star microscope.
Transmission Electron Microscopy
From the same specimens used for light microscopy
(LM), ultrathin sections of silver interference-color were
cut with a diamond knife on a LKB Ultrotome V ultramicrotome and collected on uncoated 200–300-mesh copper grids. Sections were stained with methanolic uranyl
acetate and lead citrate (Reynolds, 1963). Micrographs
were taken with a Philips CD-10 electron microscope
at 80 kV.
Scanning Electron Microscopy
Four left intact eyeballs were fixed as above indicated
for light and transmission electron microscopy (TEM),
dehydrated in graded ethanol and amylacetate, and
critical point dried in CO2. The eyeballs were cut with a
razor blade along equator and the posterior parts were
mounted on aluminum stubs, coated with gold and
examined and photographed with a Hitachi S-800 field
emission scanning electron microscope.
Morphometric Analysis
All micrographs used for the morphometric analysis
were taken from the three parts of the pecten (base,
folds, and bridge). The following four parameters were
considered: mean external diameter of the capillaries,
mean length of the luminal and abluminal microfolds
(AM), mean number, and mean area of the pigment
granules.
All data were obtained from 15 semithin or ultrathin
sections per animal (five for each part of the pecten for a
total of 60 sections), collecting one semithin section
every 100.
For the mean external diameter of the capillaries and
the mean number of pigment granules/unit area (UA)
(2,500 lm2), the sections were observed with a Zeiss
Primo Star microscope with a 40 objective and the
images were captured using a Canon A620 Powershot
camera and saved as tagged image format files with the
Adobe Photoshop CS software. All micrographs were
printed at the same final magnification of 1,000 and
were blindly assessed by three observers independently
(Pasquale Aragona, Domenico Puzzolo, Antonio Micali):
the mean and the standard deviation of the results were
recorded. The mean diameter of the capillaries was calculated only from the blood vessels which showed a
542
MICALI ET AL.
Fig. 1. Scanning electron micrograph of the pecten oculi of the budgerigar M. undulatus illustrating the
different parts of the organ: base (B), folds (F), and bridge (Br).
circular profile. A Peak Scale Loupe 7x (GWJ Company,
Hacienda Heights) micrometer was used as a scale calibration standard to calculate the diameters. 120 capillaries (40 capillaries for each part of the pecten) were
considered. The mean number of pigment granules was
calculated by counting all pigment granules observed in
one randomly chosen UA of 2,500 lm2; 120 UAs (40 UA
for each part of the pecten) were considered.
For the mean area of the pigment granules and the
mean length of the luminal and AM, TEM negative films
(Kodak 4489, 8 10 cm) were obtained at the same voltage, exposure time, and magnification. The negative
films were acquired (ratio 1:1) with an Epson Perfection
scanner and processed with a Macintosh MacBook using
the Adobe Photoshop CS software. TEM negative films
were converted into positive images at the same final
magnification of 7,500; the OPTILAB (Graphtek) software was used for the morphometric analysis. The mean
granular area was calculated as follows: the perimeter of
each granule was traced using the OPTILAB software
options, so that the included area was automatically calculated and the results, obtained in square pixels, were
converted into lm2. Forty granules/part of the pecten
(for a total of 120 granules) were measured. The mean
length of the luminal and AM was obtained only from
the capillaries provided of a circular profile. The mean
length was calculated with the OPTILAB software
options by tracing a line along the course of each microfold; the results in linear pixels were automatically
converted into lm. Sixty capillaries (20 capillaries for
each part of the pecten) were considered: for each
capillary, 10 luminal and 10 AM were measured for a
total 1,200 microfolds.
All data were expressed in lm for linear values and in
lm2 for surface values.
Statistical Analysis
Statistical analysis of the results was performed using
the Student T-test by the S.A.S./Sta 6.0.3 software. A
P value of 0.05 was considered as statistically significant.
RESULTS
Structural and Ultrastructural Data
The pecten oculi of the budgerigar is placed in the
postero-inferior wall of the eyeball, oriented cranio-caudally and postero-anteriorly, along the course of the fetal
fissure. It is 1.8–2.2-mm long, 0.6–1.0-mm high, and
0.12–0.22-mm thick: as the entire eyeball of the budgerigar has a diameter of 8–9 mm, the pecten extends for
about one-fourth of the eye. It is formed by 10–12 thin
and rectilinear folds or pleats, uniform in their external
morphology along the entire pecten. The folds are held
together in their apical part by the transverse bridge, so
that three different parts can be described: the base, the
folds, and the bridge (Fig. 1).
When viewed with the scanning electron microscopy
(SEM) (Fig. 2a), each fold originates from the retinal
surface with a thin part, the base, and then enlarges
progressively and its surface becomes round and irregular, because of the presence of the pectineal capillaries of
the folds. A transverse section of the basal part of the
pecten (Fig. 2b) shows that it corresponds to the remnants of the fetal fissure and is placed over the optic
nerve fibers. It consists of many capillaries and of two
parallel vessels, an arteriole and a venule, whose caliber
ranges between 60 and 80 lm. The wall of the basal
arteriole is formed by endothelial cells, by a single or
double layer of smooth muscle cells and by the basement
membrane (Fig. 2c). The wall of the venule is formed by
Fig. 2. Base region of the pecten oculi of the budgerigar M. undulatus. (a) Each fold (F) arises from the base (B). (b) The pecten merges
along the remnants of the fetal fissure (arrowhead); a pectineal
arteriole (A) and a venule (V), collecting some capillaries (arrows), are
evident. F ¼ fold; ONF ¼ optic nerve fibers. (c) The wall of a basal
arteriole is formed by endothelial cells (E), by smooth muscle cells
(SMC) and by the basement membrane (arrow). (d) The wall of a basal
venule is formed by endothelial cells (E) and by the basement
membrane (arrow). ONF ¼ optic nerve fibers.
544
MICALI ET AL.
Fig. 3. Fold region of the pecten oculi of the budgerigar M. undulatus. (a) The capillaries (C) show a thick wall formed by endothelial
cells (arrow). Pc ¼ pigment cell; Hy ¼ hyalocyte. (b) The tortuous
course and the uniform caliber of the superficial capillaries (arrow) is
evident with the SEM. (c) A superficial capillary shows endothelial
microfolds on both luminal (arrows) and abluminal (double arrows)
sides. The endothelial cells (inset) are connected by tight junctions
(arrowhead). BM ¼ basement membrane; ILM ¼ inner limiting membrane; Hy ¼ hyalocyte with cytoplasmic processes (*); RBC ¼ red
blood cell. (d) The cytoplasm (C) of an endothelial cell is reduced to
a thin strip; rectilinear luminal microfolds (LM) and tortuous AM are
present.
THE PECTEN OCULI OF THE PARROT
Fig. 4. Fold region of the pecten oculi of the budgerigar M. undulatus. (a) The wall of a superficial capillary is formed by an endothelial
cell provided of both luminal and AM (E1) and by two endothelial cells
with flat surfaces (E2). Arrows ¼ intercellular junctions; BM ¼ thick
basement membrane; ILM ¼ inner limiting membrane; P ¼ pericytic
processes. (b) Three interstitial pigment cells (Pc1-Pc2-Pc3), among
which wide intercellular spaces (*) can be observed. C ¼ capillaries.
545
(c) In the cytoplasm of a pigment cell large granules (PG) and mitochondria (m) are present. (d) On the external surface of a capillary (C),
a hyalocyte (Hy) is placed under the inner limiting membrane (ILM).
P ¼ pericyte. (e) An isolated hyalocyte (arrow) is placed on the fold
surface where the inner limiting membrane is interrupted. At higher
magnification (inset), the hyalocyte (Hy) shows many processes
(arrowhead).
546
MICALI ET AL.
Fig. 5. Bridge region of the pecten oculi of the budgerigar
M. undulatus. (a) The bridge (Br) is thinner on the optic nerve side,
where the folds show an oblique course (*), and wider on the ciliary
side, where the folds show an orthogonal course (**). (b) The bridge
is formed by capillaries (C) and by pigment cells (arrows). (c) Interstitial pigment cells (Pc1-Pc2-Pc3), in whose cytoplasm large granules (PG) and mitochondria (m) are present. C ¼ capillary; * ¼
intercellular spaces.
THE PECTEN OCULI OF THE PARROT
547
Fig. 6. Mean external diameter of the capillaries (expressed in lm)
in the different parts of the pecten oculi of the budgerigar M. undulatus. No statistically significant differences were found among the three
parts of the organ.
a continuous layer of endothelial cells and by the basement membrane: a layer of collagen fibers (1–1.5 lm
thick), probably derived from the mesenchyme of the
fetal fissure and exclusively placed at this site, separates
the venular wall from the optic nerve fibers (Fig. 2d).
The transverse section of a fold (Fig. 3a) demonstrates
the presence of many capillaries with a thick wall (up to
3 lm) formed by endothelial cells. Among the capillaries
many pigment cells filled with dark granules can be
observed. On the surface of each fold isolated hyalocytes
are also present. The pectineal capillaries, when viewed
with the SEM (Fig. 3b), show a uniform size and a tortuous course, so that each fold shows an irregular surface.
With the TEM (Fig. 3c), the capillaries of the pecten are
formed by endothelial cells extremely folded on both
their luminal and abluminal sides and connected by
tight junctions (Fig. 3c, inset). Endothelial cells rest on a
basement membrane, 0.15–0.25-lm thick, which, in the
superficial vessels, is in close contact either with the
long and irregular cytoplasmic projections of isolated
hyalocytes or with the inner limiting membrane. At
higher magnification (Fig. 3d), the endothelial cytoplasm
is very thin (0.2–0.3 lm) and the microfolds are long and
rectilinear on the luminal side and tortuous and shorter
on the abluminal side.
On the external surface of the folds, occasional capillaries with endothelial cells that show either both luminal
and AM or smooth surface are evident. The cells are connected by tight junctions and rest on a lamellar and
thicker (0.5–0.9 lm) basement membrane, on which
some processes of pericytes adhere (Fig. 4a).
Among the capillaries interstitial pigment cells
(Fig. 4b) delimit wide intercommunicating intercellular
spaces (0.5–1.5 lm), partially filled by thin processes.
Their cytoplasm is filled with round pigment granules
and large mitochondria (Fig. 4c).
On the vitreal surface of the pecten, between the
endothelial basement membrane and the inner limiting
Fig. 7. Mean length (expressed in lm) of the luminal and abluminal
processes of the capillaries in the different parts of the pecten oculi of
the budgerigar M. undulatus. All measurements were statistically significantly different from the others.
membrane, large (up to 15 lm in diameter) hyalocytes
are present (Fig. 4d): they show elliptical nuclei with
dispersed chromatin, a thin halo of cytoplasm and many
cellular processes. When the inner limiting membrane
lacks owing to its loose adherence to the pectineal surface, long (up to 5–7 lm) rectilinear processes adherent
to the pectineal capillaries surface can be observed with
the SEM, either at low (Fig. 4e) or at higher magnification (Fig. 4e, inset).
The bridge of the pecten (Fig. 5a) gathers the apical
ends of each fold and shows different morphological
patterns in its various parts. In fact, the folds originating from the optic nerve region are bent ciliarly and
seem to be continuous with the bridge, with only a little change on their major axis. Near the ciliary extremity, the folds are bent on their major axis, thus
penetrating the bridge with an angle of nearly 90 .
When considered as a whole, the folds form an angle of
120–130 , opened toward the outer part of the eyecup.
If viewed from above, the bridge has a triangular
shape, being thinner on the optic nerve side and wider
on the ciliary side.
A transverse section of the bridge (Fig. 5b) shows
many capillaries and a large number of pigment cells
filled with dark granules. With the TEM (Fig. 5c) the
capillaries show thick walls and a thin basement membrane, whilst the interstitial pigment cells are provided
of many round and electron dense granules, of mitochondria and of many thin processes which jut into the wide
(0.5–1.3 lm) intercellular spaces.
548
MICALI ET AL.
Fig. 8. Mean number of the pigment granules/UA (2,500 lm2) in the
different parts of the pecten oculi of the budgerigar M. undulatus. A
statistically significant difference was found among the three parts of
the organ.
Fig. 9. Mean area of the pigment granules (expressed in lm2) in
the different parts of the pecten oculi of the budgerigar M. undulatus.
A statistically significant difference was found among all parts of the
organ.
Morphometric Analysis
The morphometric analysis carried out on the mean
diameter of the capillaries reveals no statistically significant difference among the parts (Fig. 6).
The evaluation of the mean length of the luminal and
the AM of the endothelial cells demonstrates the highest
values from those present in the folds region (1.6 0.4 lm and 1.2 0.2 lm, respectively), intermediate
values from those present in the bridge (1.3 0.2 lm
and 0.9 0.2 lm, respectively), and the lowest from
those present in the base (1.1 0.3 lm and 0.8 0.1 lm, respectively). Statistically significant differences
are present among all considered groups (Fig. 7).
The mean number of the pigment granules is particularly low in the base (11.9 1.3) and higher in the folds
and in the bridge (62 4.7 and 68.6 2.9, respectively).
However, the three parts of the organ show a statistically significant difference for the number of granules
(Fig. 8).
As to the mean area of the pigment granules, the
highest value is found in the bridge (1.4 0.3 lm2),
whereas lower values (0.6 0.3 lm2 and 0.8 0.1 lm2,
respectively) are observed in the base and in the folds.
Statistically significant differences are demonstrated
among all groups (Fig. 9).
DISCUSSION
The pecten oculi is found in the vitreous chamber of
the eye of all avians (Rochon-Duvigneaud, 1943) and it
is considered an indirect retinal trophic system (Michaelson, 1954; Puzzolo, 1994), more effectively functioning
during saccadic oscillations (Pettigrew et al., 1990). It is
composed of three different parts: the base, originating
from the optic nerve head, the folds, arranged like an
inverted fan, and the bridge, running like a handrail
along the vitreous margin of the organ.
The base plays a relevant mechanic role, as it provides
strong insertion of the pecten on the adjacent ocular
layers along a zigzag line (Puzzolo et al., 1985b). This
arrangement seems to be more functional than a rectilinear one in increasing its mechanical stability and its
ability to withstand the inertial forces of the adjacent
vitreous body (Tucker, 1975). Furthermore, it represents
the site where the larger vessels (arterioles and venules)
are found (Hossler and Olson, 1984). In the budgerigar
these vessels are placed along the basal part, close to
the optic nerve fibers, so that the pecten, differently
from other avians (Kiama et al., 1994; Braekevelt, 1998;
Rahman et al., 2010), is composed only by capillaries.
As to the folds, a relationship was proposed between
the number of the pleats and the circadian activity and/
or the visual requirements of the single species (Braekevelt, 1998). In fact, a large and complicated pecten with
15–20 pleats is generally observed in photically active
and visually oriented avians, whereas a pecten provided
of smaller size and 4–5 pleats is found in avians with
crepuscular or nocturnal habits and with reduced visual
acuity. In the diurnal and visually oriented budgerigar,
an intermediate value of 10–12 pleats, similar to the
mallard (Braekevelt, 1990), was found.
The bridge has been described as a relatively thick,
pigmented, and poorly vascular plate (Tucker, 1975)
with just a mechanic role. In fact, a firm connection
between the vitreous and the pecten is generally
ensured by vitreo-capsular fibers which, in the chicken,
penetrate into the superficial microfolds of the pigment
cells (Fischlschweiger and O’Rahilly, 1968) in a sawteeth fashion (Puzzolo et al., 1985b). In the bridge of the
budgerigar no vitreal fibers are observed, so that a
THE PECTEN OCULI OF THE PARROT
mechanical role cannot be confirmed. On the contrary,
different from all the birds examined, a large number of
capillaries with thick wall are present, so that we can
suggest a relevant trophic role also for this part of the
pecten.
The main structural components common to the different parts of the pecten are the hyalocytes, the pigment
cells and the blood vessels.
The hyalocytes (Seaman and Storm, 1965; Puzzolo
et al., 1980; Ogawa, 2002) or peripectinate cells
(Fischlschweiger and O’Rahilly, 1966; Uehara et al.,
1990; Liebner et al., 1997) are placed on the vitreal
surface of the pecten. They are considered as a subtype
of blood-borne macrophages (Llombart et al., 2009) originated during embryogenesis from the primitive arteria
cupulae opticae (Liebner et al., 1997). In the budgerigar,
the hyalocytes are large cells placed under the pectineal
limiting membrane, continuous with the retinal limiting
membrane. Their position external to the vitreous body
and adherent to the pectineal surface can be the consequence of a migration from the primitive vessels during
the development. As to their distribution and number,
we are not able to demonstrate the large number of isolated or even clustered hyalocytes observed in the adult
chick (Uehara et al., 1996). It appears that, at least in
the budgerigar, the hyalocytes are generally isolated and
few in their absolute number.
The pigment cells, derived from the outer leaflet of the
optic cup, are considered as glial cells with unique morphological characteristics either during embryonic development or in the adult. During embryogenesis, a glial
epithelium with well-evident tight junctions forms a
primitive, but functional, glial blood–brain barrier
(Gerhardt et al., 1996; Liebner et al., 1997). In the adult,
the barrier function is lost (Reichenbach and Wolburg,
2005). However, the pecten glial pigment cells play other
important roles: the absorption of the sunlight (Rahman
et al., 2010), the regulation of the temperature in the
eye (Bawa and YashRoy, 1974), the flow of oxygen and
carbon dioxide between the capillaries and the vitreous
body (Jasinski, 1973), and the detoxification of the retina
by transforming vitreal ammonia into glutamine due to
a strong expression of glutamine synthetase (Gerhardt
et al., 1999). More recently, it was proposed that, in avians living in particularly difficult environmental conditions, the pigment cells of the pecten may support brain
function through a limited but critical melanin-initiated
conversion of light to metabolic energy. Therefore, a
direct correlation between the degree of melanization of
the pecten and the flight performances of the animal
was hypothesized (Goodman and Bercovich, 2008). In
the budgerigar, the morphological analysis shows a great
number of pigment cells rich in mitochondria and a
large amount of intercellular spaces (Schreck and
Bowers, 1989). The morphometric analysis provides a
strong support to the ultrastructural data as it demonstrates that the cellular area occupied by the granular
melanin is statistically significantly higher in the bridge
region, thus suggesting a great involvement of this part
of the organ in the metabolic activity of the avian eye.
It has been shown that the pectineal vessels are
formed by lymphatic vessels (Scala et al., 2002; Corona
et al., 2004) and by blood capillaries (Braekevelt, 1988).
In fact, in the pecten of Anas plathyrhynchos (Scala
et al., 2002) lymphatic vessels, which might drain retinal
549
catabolites from the vitreous body (Corona et al., 2004),
are demonstrated with the SEM analysis of vascular
casts. In our study, we are able to identify only the presence of large intercellular spaces, whereas no lymphatic
vessels are evident in the budgerigar.
As to the blood capillaries, they are characterized by a
maximum increase of the surface of the endothelial cells
at the minimum thickness of their walls (Jasinski,
1973). In fact, even if apparently thick with the LM,
they are formed by a thin strip of cytoplasm and, on
both the luminal and abluminal surfaces, by a large
number of microfolds (Braekevelt, 1988; Kiama et al.,
1998) showing a great variability in number, length, and
organization with the TEM. In the budgerigar, pleated
membranes are present on both luminal and abluminal
surfaces nearly in all endothelial cells; the luminal
microfolds are generally rectilinear, whereas the AM are
always tortuous. The presence of the microfolds determines an enormous enlargement of the inner and outer
surfaces of the vessels. The demonstration of carbonic
anhydrase activity in the apical and basal microfolds of
the pectineal endothelial cells (Eichhorm and Flugel,
1988) indicates that the pecten may play a significant
role in the intraocular pH regulation, as already suggested by Brach (1977) after experimental destruction of
the pecten and by Gerhardt et al. (1999) during its
development. Furthermore, as it was shown that the
pectineal endothelial cells possess an extraordinarily
high amount of glucose transporter isoform-1 (Gerhardt
et al., 1999), it is possible to propose that in the budgerigar the folds region, characterized by the longest luminal and AM, may have a trophic role as a glucose
provider to fuel the glycolysis of the avascular retina
(Wolburg et al., 1999). Conversely, the bridge region,
where the number and the area of the pigment granules
show the highest values, seems to be more involved in
the production of energy.
This study shows that morphometric analysis, used
together with morphological features, allows a more
precise description of a complex structure such as the
pecten oculi in the budgerigar, giving hints about the
possible functional roles of the different parts of the
organ.
ACKNOWLEDGEMENTS
The authors thank Mr. Sebastiano Brunetto of the
Department of Biomorphology and Biotechnologies (University of Messina, Italy) for the technical assistance. All
the authors declare no commercial relationships relevant
to the subject matter of the article.
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melopsittacus, morphometric, undulatus, stud, pecten, morphological, oculo, budgerigar
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