The eyes of suckermouth armoured catfish (Loricariidae, subfamily Hypostomus): pupil response, lenticular longitudinal spherical aberration and retinal topography
1 Applied Vision Research Centre, Department of Optometry & Visual
Science, City University, Northampton Square, London EC1V 0HB, UK
2 Department of Anatomy & Developmental Science, School of Biomedical
Science, The University of Queensland, Brisbane 4072, Queensland,
Australia
3 Anatomisches Institut, Universität Tübingen,
Österbergstrasse 3, Tübingen, 72074, Germany
* Author for correspondence (e-mail: r.h.douglas{at}city.ac.uk)
Accepted 8 August 2002
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Summary |
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Key words: catfish, pupil, retina, iris, aberration, Liposarcus pardalis, Pterygoplichthys etentaculus
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Introduction |
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The aim of the present study was to quantify the pupil responses of another
group of teleosts; the suckermouth armoured catfish, which belong to the
Loricariid family of Siluriform catfish resident in the freshwaters of Panama
and South America. Specifically, we investigated members of the subfamily
Hypostomus, which, along with some other members of the Loricariidae, are
popularly referred to by the generic name `Pleco' or `Plecostomus', but, in
fact, comprise over 100 species in approximately 18 genera
(Nelson, 1994). This group was
chosen for study because Walls
(1963
) suggested that they may
show extensive pupil mobility, although no details of the extent and speed of
migration were provided. Clearly, however, the pupil responses of these
catfish will be very different to those of P. notatus, because
although the fully dilated pupil is, as in most other vertebrates, round, when
constricted it takes on the shape of a `crescent moon' owing to the presence
of a dorsal iris operculum.
Iris opercula are common among some elasmobranch fish, such as skates and
batoid rays (Beer, 1894; Franz,
1905
,
1931
;
Young, 1933
;
Walls, 1963
;
Kuchnow and Martin, 1970
;
Kuchnow, 1971
;
Gruber and Cohen, 1978
;
Nicol, 1978
;
Collin, 1988
), and also occur
in some bottom-dwelling teleosts (Bateson,
1890
; Beer, 1894
;
Walls, 1963
;
Munk, 1970
;
Collin and Pettigrew, 1988a
;
Nicol, 1989
). Despite the
relatively widespread occurrence of such asymmetric pupils, their function
remains uncertain. One explanation is that they may reduce the effect of any
longitudinal spherical aberration the lens might possess by restricting light
to the lens periphery (Murphy and Howland,
1991
). Most fish suffer little from longitudinal spherical
aberration owing to a refractive index gradient within the lens (see
Sivak, 1990
for a review).
However, if crescent-shaped pupils do function primarily to reduce such
aberration, one might expect the lenses of animals with these pupils to be
poorly corrected for it. We therefore determined the longitudinal spherical
aberration of the lens in a species of suckermouth armoured catfish.
Finally, the retinal ganglion cell topography of these catfish was
assessed. Although few studies have investigated the density of retinal
ganglion cells with crescent-shaped pupils, the crescent-shaped iso-density
contours in retinal wholemounts of the sharp-nosed weaver Parapercis
cylindrica (Teleostei; Collin and
Pettigrew, 1988a) and the shovel-nosed ray Rhinobatos
batillum (Elasmobranchii; Collin,
1988
) in conjunction with a similarly shaped pupil suggest that a
relationship may exist.
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Materials and methods |
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Measurement of pupil response
Three individual Liposarcus pardalis Castelnau 1855 [standard
lengths (SL) 140-150 mm] were held in a 12h:12h L:D cycle for at least 3
months. To examine their pupil response, they were removed from their home
tanks during the dark phase of their L:D cycle using a dim red torch and
placed in a small aquarium. Following 1 h of acclimation to this tank,
pupillary responses were filmed for 60 min using infrared illumination during
continual exposure to one of 13 intensities of white light. Each fish was
examined at the same time each day to avoid any circadian influences on the
pupil response, receiving only one light exposure per day. As these animals
naturally tend to stay motionless in the light, the only form of restraint
necessary during filming was a Perspex `tent' placed over them. Stimuli were
delivered from directly overhead, via a shutter-controlled opening and a
mirror, from a Kodak projector located in an adjacent room, which also housed
all recording apparatus. The intensity of illumination was controlled by
neutral density filters. One eye of each animal was videotaped using an
infrared-sensitive camera (Cohu, San Diego, USA) positioned in a plane
parallel to the cornea. Pupil area was subsequently determined from individual
video frames using NIH-image. To facilitate comparison among individuals of
different eye size, all measurements were expressed relative to the fully
dilated pupil area of each animal just prior to experimental light
exposure.
Determination of lens longitudinal spherical aberration
Following immersion in a lethal dose of methane tricaine sulfonate salt (MS
222), both lenses were removed from a single Pterygoplichthys
etentaculus Spix and Agassiz 1829 (SL 200 mm). P. etentaculus,
whose pupil is also crescent shaped when constricted, was preferred to L.
pardalis for this part of the study owing to its larger size. The lenses
of P. etentaculus, which, like those of other suckermouth catfish
(L. pardalis, Glyptoperichthys lituratus and
Sturisomatichthys sp.; R. H. Douglas and S. P. Collin, unpublished
data), are anteroposteriorly flattened, were glued to the tip of a fine
pipette, placed in a small glass tank and immersed in a teleost Ringer
solution containing small amounts of scatter liquid concentrate (Edmund
Scientific, Barrington, USA). The beam of an HeNe laser (emission
maximum 632.8 nm) was then passed through the lens along the antero-posterior
axes. A camera positioned at the side of the lens was used to ensure that the
laser beam passed through its vertical midpoint. This was achieved by
adjusting the height of the laser beam until it was not deflected by the lens
from the horizontal plane. The laser beam was then filmed from above while
traversing the lens in the horizontal plane. Individual video frames were
analysed using software to determine the back vertex distance (BVD) for a
number of beam entry positions. A non-linear regression was applied to the
data using the following equation for back vertex distance (x):
x=a+by2+cy4, where
a represents back vertex focal length, b represents the 3rd
order spherical aberration, c represents the 5th order spherical
aberration, and y represents the normalised beam entry position. This
equation represents the longitudinal ray aberration of a rotationally
symmetric optical system on axis.
Retinal structure and ganglion cell topography
The eyes of a single L. pardalis (SL 220 mm) were embedded in
resin for light microscopy, and two interrupted series of 0.5 µm sections
were cut on an ultramicrotome and stained with Toluidine Blue. One eye was
serially sectioned in the dorso-ventral axis and the other along the
naso-temporal axis.
Both eyes of two individuals of Liposarcus multiradiatus Hancock, 1828 (SL 88 mm) and one L. pardalis individual (SL 158 mm) were used for topographic analyses of retinal ganglion cell distribution. After 3 h of dark adaptation and immersion in a lethal dose of MS 222, eyes were enucleated with at least 2-3 mm of the optic nerve still attached. Extraocular muscle tissue was removed, with care taken not to puncture the eyecup. While immersed in oxygenated teleost Ringer solution, a further 1-2 mm of the optic nerve was removed, and the remaining nerve stump swabbed dry with a tissue wick. Crystals of fluorescein-conjugated dextran (3000 MW, anionic, lysine-fixable; Molecular Probes, Leiden, The Netherlands) were then applied to the entire diameter of the lesioned optic nerve. After approximately 5 min, to allow uptake of the dextran label, the whole eye was re-immersed in oxygenated Ringer solution for 24 h at 21°C.
Following incubation, the limbus of each eye was pierced and the cornea and lens were removed. A small dorsal incision was made in the retina for orientation. The eyecup was immersion fixed in 4% paraformaldehyde in 0.1 mol l-1 phosphate buffer (pH 7.4) for 40 min before dissection in 0.1 mol l-1 phosphate buffer. Each retina was removed from its scleral eyecup and wholemounted (ganglion cell layer uppermost) on a subbed slide (double-dipped in 5% gelatin), covered in either Fluoromount (Calbiochem, San Diego, USA) or 0.1 mol l-1 phosphate buffer and coverslipped. Dehydration was inhibited by sealing the edges of the coverslip with nail polish. One retina of L. multiradiatus was wholemounted and prepared as above but left overnight in a humidified Petri dish before being stained for Nissl substance with 0.05% Cresyl Violet for 3 min. The wholemount was then dehydrated in a series of alcohols and mounted in DPX to reveal the distribution of glial cells.
Topographic analysis of the retrogradely labelled ganglion cells was
carried out following the protocol of Collin and Northcutt
(1993), where up to 200
regions per retina (50-60% of the retinal area) were sampled, allowing small
fluctuations in density to be noted. Iso-density contours were constructed by
joining areas of similar cell density. Retinal shrinkage was assumed to be
minimal because all retinae were examined while hydrated. The total number of
labelled ganglion cells was calculated by multiplying the average cell density
between each iso-density contour by its area. Area measurements were
calculated by scanning the topography map into a PC and analysing the area of
each contour using NIH-Image. Retrogradely labelled ganglion cells were viewed
and photographed on a Zeiss Axiophot 135M fluorescence microscope (Jena,
Germany) fitted with a fluorescein filter block using Kodak Tmax 400 ASA
film.
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Results |
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Pupillary constriction in L. pardalis consists of two components; a general reduction in the diameter of the pupil and the outgrowth of an operculum from the dorsal margin of the iris (Fig. 3). Consequently, while the fully dilated pupil of L. pardalis is more or less round (Fig. 4A), when constricted it appears as a `crescent moon' with an irideal flap obscuring the central pupil (Fig. 4B). In general, especially at higher light levels, the decrease in overall pupil diameter occurs more rapidly than the increase in opercular area (Fig. 3).
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Longitudinal spherical aberration of the lens
The lenses of P. etentaculus are well corrected for longitudinal
spherical aberration, showing only relatively small differences in back vertex
distance (BVD) for laser beams passing through the lens at different points
and displaying a balance between negative 3rd order and positive 5th order
aberrations (Fig. 5). The
maximum difference in BVD for beams passing through the lens at different
points within the lens is approximately 10% of the total focal length.
|
Retinal structure
In the isolated eyecup of all the various species of armoured catfishes
examined, an elongated embryonic fissure extends from the central retina to
the ventral margin. The choroid protrudes through the fissure to form a
falciform process, which gives rise to an extensive system of vitreal blood
vessels. In radial sections examined by light microscopy, the photoreceptors
of the L. pardalis retina are exclusively single cones interspersed
with elongate rods (Fig.
6).
|
Multiple optic nerve head papillae
Histological sections cut parallel to the embryonic fissure reveal several
discrete optic discs (papillae) running along the fissure. Ganglion cell axons
backfilled with fluorescein-conjugated dextran, which are dispersed relatively
evenly in peripheral retina, form discrete bundles or `fascicles' as they
approach the embryonic fissure (Figs
7A-C,
8). The thickness of each
fascicle varies from 12 µm to 80 µm in diameter
(Fig. 7D), and up to six
fascicles may converge to form a single optic papilla
(Fig. 7A,B). The optic nerve
head, therefore, comprises a series of optic papillae, each fascicle
converging from either unilateral or bilateral regions of the retina. At the
dorsal end of the optic nerve head, the fascicles converge from temporal,
dorsal and nasal retinal regions. Although predominantly located in the
ganglion cell layer and separated from the optic fascicles, the retinal
ganglion cells form loosely distributed columns lying between each optic
fascicle (Fig. 8). In Cresyl
Violet-labelled retinae, well-defined glial columns also emanate from the
elongated series of optic nerve heads like the spokes of a wheel.
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Retinal ganglion cell topography
Retrogradely labelled ganglion cells are distributed non-uniformly
throughout the retina. Peaks in ganglion cell density, or areae
centrales, lie on each side of the vertically oriented falciform process,
just dorsal of the horizontal meridian. In L. pardalis, densities
peak at 18.6x102 cells mm-2 and
24.2x102 cells mm-2 in nasal and temporal retinal
regions, respectively (Fig. 9).
In L. multiradiatus, densities are similar, with
18.6x102 cells mm-2 and 16.4x102
cells mm-2 in nasal and temporal retinal regions, respectively.
Although not analysed topographically, a small population of displaced
ganglion cells that lie in the inner nuclear layer were also labelled with a
peak density of 2.5x102 cells mm-2 in L.
multiradiatus. The total number of retinal ganglion cells that lie either
within the ganglion cell layer or within the inner nuclear layer in L.
pardalis is 33 000.
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Discussion |
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However, the greatest difference between the pupil response dynamics of
P. notatus and L. pardalis is in the speed of migration. As
in humans and many other vertebrates, the t0.5max in
P. notatus occurs in less than one second, while in L.
pardalis the t0.5max is in the order of several
minutes, with full constriction usually taking 35-45 min. The responses
recorded here for L. pardalis are again similar in their time course
to those observed in nocturnal elasmobranchs
(Kuchnow, 1971;
Douglas et al., 1998
).
Function of pupil closure
In most lenses, light rays entering at different eccentricities will be
focused at different distances behind the lens, inevitably blurring the image
on the retina. In most terrestrial animals, the effects of longitudinal
spherical aberration within the lens are minimised, as the cornea is the major
refractive surface and the pupil can constrict to limit passage of light to
only part of the lens. Lens quality, although important to any visual animal,
is much more an issue for fish, as the cornea is effectively neutralised
underwater, resulting in the lens being the only refractive surface, and in
most species the lens protrudes through an immobile pupil with the whole lens
consequently being involved in image formation. The degree of longitudinal
spherical aberration recorded for fish lenses varies between species and with
the age of the animal (Sivak,
1990). However, not surprisingly, the lens is generally well
corrected for such aberration through the possession of a refractive index
gradient (Sroczynski, 1976
,
1978
,
1979
,
1981
;
Sivak and Kreuzer, 1983
;
Fernald and Wright, 1983
;
Kreuzer and Sivak, 1984
;
Jagger, 1992
;
Kröger and Campbell,
1996
; Kröger et al.,
1994
,
2001
;
Garner et al., 2001
). The
degree of aberration observed here for the catfish is comparable with that
recorded for other fish with immobile pupils. This suggests that it is
unlikely that the main purpose of the mobile crescent-shaped pupil is to
decrease the effects of longitudinal spherical aberration. This is in line
with the observation reported for the clearnose skate Raja elanteria,
which also has a crescent-shaped pupil yet displays very little longitudinal
spherical aberration (Sivak,
1991
; Sivak and Luer,
1991
).
We have previously suggested that, since the majority of teleost fish with
extensive pupil mobility are bottom-dwelling animals that attempt to blend in
with the substrate, the constriction of the pupil may aid in camouflaging the
animal through obscuring the otherwise very visible pupil
(Douglas et al., 1998). The
same argument could be applied to L. pardalis and other
bottom-dwelling suckermouth catfish, as the irideal operculum distorts the
shape of the eye and blends with the rest of the fish's body markings when
viewed by potential predators from above. The animal would, however, be able
to maintain vision through its crescent-shaped pupil in the anterior,
posterior and ventral directions, with two areas of increased acuity examining
the substrate in front of and behind the animal (see below).
Retinal morphology
In agreement with other studies on catfish
(Ali and Anctil, 1976;
Nicol, 1989
;
Pavan, 1946
;
Wagner, 1970
;
Ali and Wagner, 1975
; Verrier,
1927
,
1928
;
Douglas and Wagner, 1984
;
Nag and Sur, 1992
;
Sillman et al., 1993
), the
retina of L. pardalis is composed of single cones and large rods
(Fig. 6). Double cones, which
are present in most teleosts, appear to be absent from these species. This is
surprising, as catfish often inhabit what could be classed as low-light-level
environments and might therefore be expected to have retinae `designed for
sensitivity'. Thus, many catfish, for instance, have a retinal tapetum
lucidum, a feature thought to enhance photon capture
(Nicol et al., 1973
;
Arnott et al., 1974
). There is
evidence that double cones are a further mechanism for enhancing sensitivity.
Ontogenetic development of double cones, for instance, is often associated
with a change in lifestyle from brightly lit surface waters to inhabiting
dimmer, deeper waters (e.g. Boehlert,
1978
), and psychophysical experiments in birds suggest that double
cones code for luminosity rather than being involved in colour vision
(Maier and Bowmaker, 1993
).
Thus, one might expect large numbers of double cones in catfish rather than
their complete absence. However, there is circumstantial evidence that double
cones are involved in movement detection in both birds
(Campenhausen and Kirschfeld,
1998
) and fish (Levine and
MacNichol, 1982
), especially when arranged in a square mosaic
(Collin and Collin, 1999
). The
propensity of catfish to feed on non-mobile prey in generally turbid water may
account for the lack of double cones. Alternatively, double cones seem to have
a role in mediating polarisation sensitivity
(Hawryshyn, 2000
), an ability
that catfish might therefore not possess.
As in members of most catfish families
(Deyl, 1895; Ströer,
1939; Herrick, 1941
;
Wagner, 1970
;
Arnott et al., 1974
;
Ali and Anctil, 1976
;
Wagner et al., 1976
;
Frank and Goldberg, 1983
,
Dunn-Meynell and Sharma, 1987
;
Nag and Sur, 1992
), the
retinal ganglion cell axons of suckermouth catfish form discrete fascicles
within the nerve fibre layer, leading to multiple optic papillae. The
functional significance of this arrangement is unknown but a number of
theories have been presented to explain the existence of multiple nerve heads
in catfish. These include reducing the size of a large scotoma into several
smaller scotomata (Walls,
1963
; Dunn-Meynell and Sharma,
1987
), reducing image degradation, which may be evident as light
travels through the thick layers of optic fibres near a large optic nerve head
(Wagner, 1970
), and enhancing
stimulus perception (Walls,
1963
). Although breaking up the large scotoma resulting from a
single papilla into small, less-obtrusive scotomata may be advantageous, the
fact that the optic papillae in L. pardalis are not dispersed as in
other catfish (e.g. the channel catfish Ictalurus punctatus;
Dunn-Meynell and Sharma, 1987
)
suggests that this novel arrangement is associated with the topographic order
of axons as they enter the optic nerve
(Dunn-Meynell and Sharma,
1988
).
Retinal topography
A variety of patterns of peaks in retinal ganglion cell density have been
found in a range of teleosts (Ito and
Murakami, 1984; Collin and Pettigrew,
1988a
,b
;
Collin, 1999
) and
elasmobranchs (Hueter, 1991
;
Collin, 1988
;
Bozzano and Collin, 2000
). The
nasal and temporal areae centrales in L. pardalis and L.
multiradiatus would provide increased sampling, and therefore increased
spatial resolving power, in the rostro-ventral and caudo-ventral axes,
respectively. The arrangement of iso-density contours broadly follows the
shape of the pupil, where the retinal region underlying the operculum
possesses relatively low densities of ganglion cells, creating a high
centro-peripheral density gradient of more than 25:1
(Fig. 9). Similarly, the lack
of a dorsal pupillary operculum is also reflected in the topographic
distribution of retinal ganglion cells in I. punctatus.
Using horseradish peroxidase as a retrograde tracer from the optic nerve,
Dunn-Meynell and Sharma (1987
)
revealed a naso-temporal elongation of iso-density contours with a continuous
peak of >1.5x102 cells mm-2 lying across the
dorsal hemifield. The decrease in ganglion cell density underlying the
operculum in L. pardalis is not present, which is indicative of an
increased dependence on scanning a wider panoramic visual field in I.
punctatus. A similar relationship to that seen in L. pardalis
occurs in the eyes of the sharp-nosed weaverfish Parapercis
cylindrica (Collin and Pettigrew,
1988a
) and the shovel-nosed ray Rhinobatos batillum
(Collin, 1988
), where the shape
of a crescent-shaped pupil is reflected in the distribution of ganglion cells,
with two areae divided by a region of low density. Interestingly, the
pupils of many cetacea (Kröger and
Kirschfeld, 1993
) and some elasmobranchs
(Douglas et al., 1998
) close
down to two roughly horizontally aligned pinholes, and both of these groups
also often have two retinal areas of maximal resolution (cetacea
Dral, 1983
;
Mass and Supin, 1995
;
Murayama et al., 1995
;
Murayama and Somiya, 1998
:
elasmobranchs Peterson and Rowe,
1980
; Bozzano and Collin,
2000
; Collin,
1999
).
However, it is in many ways surprising to find such similarity between
ganglion cell distribution and pupil shape, as the pupil functions as an
aperture stop and not a field stop. So it is perhaps not unexpected that a
similar topographic regionalisation of the retina into two areae is
found in a number of elasmobranchs
(Peterson and Rowe, 1980;
Bozzano and Collin, 2000
;
Collin, 1999
; L. Litherland
and S. P. Collin, unpublished data) that appear not to have a pupillary
operculum or double pinhole apertures, suggesting that the need to optimise
acuity in the frontal and caudal visual axes may be the driving force behind
the development of retinal cell gradients rather than the presence of an
irregular pupil.
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Acknowledgments |
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