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First published online October 18, 2006
Journal of Experimental Biology 209, 4262-4272 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02499
Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra
Vision Touch and Hearing Research Centre, School of Biomedical Sciences, University of Queensland, Brisbane QLD 4072, Australia
* Author for correspondence (e-mail: S.Kleinlogel{at}uq.edu.au)
Accepted 8 August 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: underwater polarization vision, photoreceptor, compound eye, retina, e-vector, communication
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Waterman, 1981). Polarization
vision, as opposed to polarization sensitivity (PS) of the retina, is the
ability to discriminate between two lights of the same luminous intensity but
of different e-vector orientation (
) and/or degree of polarization
(Kirschfeld, 1973).
Behavioural experiments have shown that gonodactyloid stomatopods possess
polarization vision as they can discriminate two light sources on the basis of
(Marshall et al.,
1999).
Gonodactyloid stomatopods of the species Gonodactylus chiragra are
typically found in rocky inshore habitats in the low intertidal zone, where
they are exposed to high light intensity
(Caldwell and Dingle, 1976).
Here, close to the water surface, the polarization pattern of the sky can
still be seen within Snell's window
(Horváth and Varjú,
2004). Outside this aerial window, the polarized light field
produced by scattering and reflectance within the water itself is
predominantly horizontal and therefore provides a predictable background
(Cronin and Shashar, 2001;
Waterman, 1981). These
relatively consistent environmental stimulus conditions favour the evolution
of underwater polarization vision, the most general function of which is
contrast enhancement (Bernard and Wehner,
1977). However, polarization vision is probably also used for
tasks such as communication (Lythgoe,
1971; Lythgoe,
1979; Lythgoe and Hemmings,
1967; Shashar et al.,
2000; Shashar et al.,
1998). Many stomatopod species possess polarized body markings
which, like colour signals, are displayed in behavioural contexts that seem
clearly linked to intraspecific signalling
(Cronin et al., 2004;
Cronin et al., 2003).
The stalked apposition compound eyes of gonodactyloid stomatopods are
subdivided into a dorsal and a ventral hemisphere bisected by an equatorial
band of six distinct rows of enlarged ommatidia, termed the mid-band (MB;
Fig. 1). The structure of the
fused rhabdoms in both, the MB and the hemispheres is based on a two-tiered
design, typical of many crustaceans
(Nässel, 1976;
Strausfeld and Nässel,
1981). There is a relatively short 8th retinula cell (R8 cell) as
the top tier, and this overlies a longer tier, the main rhabdom, constructed
by retinula cells R1-R7 (Fig.
2A). In the hemispheres and MB rows 5 and 6, the R1-R7 cells
contribute to the entire length of the main rhabdom, whereas in MB rows 1-4
this main rhabdom is subdivided into a distal (D) and a proximal (P) tier
(Fig. 2). The MB rows will
hereafter be referred to simply as `rows'.
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).
Photoreceptors of the two groups are therefore expected to be sensitive to
orthogonal e-vector orientations of light
(Waterman, 1981). In rows 5
and 6 the microvilli within each cell group possess an especially high degree
of alignment and the microvillar layers are only 5-6 microvilli deep
(Fig. 2A). This precise
arrangement suggests increased linear PS in these rows compared to hemispheric
receptors, where the microvillar layers are 8-9 microvilli deep and less
crystalline in arrangement (Marshall et
al., 1991a; Snyder,
1973; Stowe,
1983). In contrast, the individual photoreceptors of rows 1-4
produce microvilli in both orthogonal directions, as do R8 cells
(Marshall et al., 1991a). The
microvillar layers are here uneven and disorganized, which theoretically
decreases PS drastically. In rows 1-4 Group I and Group II photoreceptors form
separate rhabdomal tiers (Fig.
2) and are sensitive to different wavelengths of light. The total
of eight spectral sensitivities within the main rahbdoms of MB rows 1-4 covers
the spectrum from 400 nm to 725 nm continuously and the UV range down to 300
nm is included via the overlying R8 cells
(Cronin and Marshall, 1989a;
Cronin and Marshall, 1989b;
Cronin et al., 1994b;
Marshall and Oberwinkler,
1999). Rows 2 and 3 are equipped with long-pass coloured filters
between the rhabdomal tiers (intrarhabdomal filters) in order to shift their
spectral sensitivities to longer wavelengths
(Fig. 2)
(Marshall et al., 1991b).
Owing to this diversity in spectral sensitivity it was proposed that
photoreceptors within rows 1-4 are involved in colour vision and they will
hereafter be referred to as `colour receptors'.
Many insects are equipped with a specialized retinal area for polarization
vision, the so-called dorsal rim area. In general, crustaceans lack such a
specialized area for polarization vision and their inherently polarization
sensitive photoreceptors are distributed homogeneously across the retina
(Eguchi and Waterman, 1966;
Shaw, 1966;
Waterman and Fernandez, 1970).
This study shows an exception to the general rule. Although Gonodactylus
chiragra possesses `typical crustacean' polarization receptors in both
hemispheres, we found specialized polarization receptors with a much higher PS
exclusively in rows 2D, 5 and 6 of the MB. They will hereafter be referred to
as `high PS cells'. The `high PS cells' are sensitive to two orthogonal
e-vector directions of polarized light and their narrow spectral sensitivities
peaking at 565 nm are well suited to detect polarized body markings displayed
by a variety of stomatopod species (Cronin
et al., 2004; Cronin et al.,
2003).
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Materials and methods |
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Stimulation
The light stimulus was produced by a 150 W xenon-arc lamp (Oriel,
Stratford, USA) in combination with a computer-controlled monochromator
(Oriel, Stratford, USA). A slit-width of 1.24 mm was used, which produced
light of a spectral composition with approximately 4 nm halfwidth (information
given by Oriel). The grating of the monochromator could be bypassed by a
front-surface-mirror in order to provide white light. The light beam was first
passed through a circular, computer-controlled neutral density wedge (Edmund
Optics, Barrington, USA) for intensity variations covering a range of four log
units and then through an electronic shutter (Melles-Griot, New York, USA).
The light was focused into a flexible UV-transmitting liquid light-guide, the
other end of which was mounted on a cardan arm perimeter device, providing a
stimulus of 0.9° for a stomatopod eye mounted in the centre of the
arrangement. The cardan arm arrangement allowed adjustment of the angular
position of the light stimulus around the preparation, yet maintained a fixed
distance between eye and stimulus. Between the end of the light guide and the
eye a broad-band (350 nm-750 nm) grey (ND
0.2) linear polarization filter
(27340 Polarizer, Oriel, Stratford, USA) could be inserted and its angle
relative to the eye changed in 10° steps. The transmission of the optical
system was calibrated with an USB 2000 spectrometer (Ocean Optics, Dunedin,
Florida, USA), which was itself calibrated against a secondary NIST standard
lamp (Oriel, Stratford, USA). At the location of the eye the white light had
an unattenuated maximal intensity of approximately 1018 photons
s-1 cm-2 and the degree of polarization of the stimulus
with the linear polarization filter in place exceeded 98% over the spectral
range from 400 nm to 720 nm.
Preparation and recording
An eye was mounted on a plastic rod with the help of a low-melting-point
bee's wax/dental wax mixture (kindly supplied by S. B. Laughlin). A small hole
(about five facets across) was cut with a razor blade in either the dorsal or
the ventral hemisphere, the rod was then placed in a glass bubble filled with
stomatopod saline (Watanabe et al.,
1967), which was placed at the centre of the cardan arm
arrangement with the MB oriented horizontally
(Fig. 1A). A microelectrode was
lowered vertically through the corneal hole and into the retina. The entire
procedure was performed under photographic safelight to avoid excessive light
adaptation of photoreceptors.
Photoreceptors were impaled using thick-walled borosilicate microelectrodes
either filled with 1 mol l-1 KCl (40-100 M
) or 5% Lucifer
Yellow CH (Sigma-Aldrich Pty Ltd, Castle Hill, NSW, Australia) in 0.1 mol
l-1 Tris buffer and 1 mol l-1 LiCl (150-300 M).
The pipette was connected to the headstage of an intracellular amplifier
(Axoprobe 1A, Axon Instruments Ltd, Inverurie, Scotland) via a
chloride silver electrode and an Ag/AgCl pellet immersed in saline served as
ground electrode. The amplified intracellular signals from photoreceptors were
monitored on a digital oscilloscope (Tektronix, Brighton, East Sussex,
UK).
Experimental protocol and evaluation of data
Upon impalement of the photoreceptor, the photoreceptor was activated with
short flashes of white light and the light source was approximately aligned
with its optical axis by moving it to the position that elicited maximal
response. Only photoreceptors with a response of at least 30 mV to white light
were investigated further. First the photoreceptor was characterized by its
spectral sensitivity, which was measured using the spectral scan method
(Menzel et al., 1986). In this
method, a photoreceptor is clamped to a preselected DC potential (criterion
response) by adjusting the light flux via the neutral density wedge
(ND) during changes in spectral content as delivered by the monochromator. The
spectral sensitivity function S(
) of the cell is given by the
reciprocal of the number of quanta of each wavelength required to maintain the
criterion depolarization (Menzel,
1979). At least three scans with varying criterion responses were
recorded for each photoreceptor and averaged. The analysis was performed using
ASYST software (Keithley Instruments Inc., Cleveland, Ohio, USA).
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max)
and minimal (min) response, respectively, were then determined
more accurately by a second run in which the polarizer was turned in steps of
10° around the maximum (max-20°,
max-10°, max, max+10°,
max+20°) and the minimum (min-20°,
min-10°, min, min+10°,
min+20°). From previous anatomical investigations it was
assumed that all data fall into groups at +45, -45, 90 and 0 degrees
(Marshall et al., 1991a) and
max and min were therefore allocated to one of
the above anatomical groups. Two response-intensity (R-log I)
functions were then recorded by applying 0.25 log intensity series of flashes
of white light. The first R-log I function was recorded with the
polarizer positioned in the direction found to generate maximal response
(max) and a second curve with light polarized in the
perpendicular direction (min), which elicited minimal response
(Fig. 3C). No baseline shift
was allowed between the two R-log I function measurements. Single
photoreceptor responses were digitised on a virtual oscilloscope (ADC-100)
using Pico Scope software (Pico Technology, Camperdown, NSW, Australia) and
then exported into Excel for analysis. All R-log I curves were fitted
to standard Rushton intensity-response functions
(Naka and Rushton, 1966a;
Naka and Rushton, 1966b) using
SigmaPlot 5.01 software (Systat Software, Hounslow, London, UK). Polarization
sensitivity (PS) is defined as the ratio between maximal and minimal
sensitivity of the photoreceptor to e-vector orientation and can be determined
from the intensity shift 
i between the two fitted R-log I
curves (Fig. 3C)
(Dacke et al., 2002):
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It is important to note that PS was probably slightly underestimated in
some recordings because the minimal angle the polarizer could be turned was
10° and max and min were therefore
determined with an accuracy of only ±5°. However, e-vector-response
curves are approximated sine-curves, which flatten around their minimum and
maximum. The inaccuracy of max and min would
result in a PS for example of 3.2 (6.0) instead of 3.5 (7.1), which does not
influence the qualitative findings of this study.
At the end of each recording some cells were iontophoretically marked with Lucifer Yellow CH (Sigma Aldrich Pty Ltd, Castle Hill, NSW, Australia) using a 0.2 to 0.7 nA hyperpolarizing DC current at 1 Hz for 8 min.
Histology
Eyes were fixed in 4% paraformaldehyde and 30% sucrose in 0.1 mol
l-1 phosphate buffer for 2-3 days at room temperature. The tissue
was dehydrated in ethanol and embedded in 2-hydroxyethylmethacrylate
(Technovit T7100, Heraeus, Germany). Serial frontal sections of 7 µm
thickness were then cut on a historange microtome (LKB) and viewed under a
Zeiss Axioscope microscope equipped with a digital SPOT camera using
fluorescent microscopy and ALPHA Vivid standard Lucifer Yellow XF14 filters
(Omega Optical, Inc., Brattleboro, VT, USA). Images were processed and the
contrast enhanced using Adobe Photoshop 7.0 (Adobe Systems).
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Results |
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) when observed in serial light microscopic sections through
the retina (Fig. 4B). The
spectral characteristics of the stained photoreceptors and the order of
impalement by the electrode were used to identify cells that have not been
stained.
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Polarization sensitivity
Stomatopod photoreceptors can be divided into four groups according to
their PS and anatomical position (Fig.
3A, Fig. 5).
Thereby we assumed that within each ommatidial row, photoreceptors of the same
cell group (R8; Group I, Group II) are identical in terms of their
physiological properties (for an overview see
Table 2). An exception is row
2D, which will be commented on later.
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Lucifer Yellow injections confirmed that the UV-sensitive photoreceptors
are R8 cells (Marshall and Oberwinkler,
1999). All UV-sensitive cells (N=17) exhibited negligible
PS values of <2. None of the R8 receptors of rows 5 and 6 was stained and
it thus remains unclear if our results include any recording from these cells.
Rows 5 and 6 R8 cells are of interest because they form unidirectional
microvilli and PS is therefore expected
(Marshall et al., 1991a). The
photoreceptors of the dorsal and ventral hemispheres, which have a `typical
crustacean' design, had an average PS of 3.8±1.6 (mean ± s.d.,
N=17). The colour receptors, as expected from structure, had
generally small PS values of 2.3±1 (N=22). However, individual
photoreceptors within row 2D were an exception. They had PS values of
6.2±1.3 (N=6), significantly higher (t-test,
P<0.01) than the PS values measured for any other `colour
receptor', including row 2P receptors. The PS values of 2D receptors equalled
the high PS values measured for photoreceptors of rows 5 and 6, which are
6.7±2.5 (N=8). Therefore photoreceptors of rows 2D, 5 and 6
are hereafter grouped together as `high PS cells' with an average PS of
6.1±2 (N=14). `High PS cells' are significantly more sensitive
to polarized light than hemispheric receptors (t-test,
P<0.005).
Re-examination of electron microscopic investigations of the structure of rhabdom 2D revealed that the microvilli in this rhabdom are more organized than in the other row 1-4 rhabdoms. In row 2D each photoreceptor almost certainly produces microvilli in only one direction and the orthogonal layers are of equal thickness, albeit three times thicker (16-17 microvilli deep) than in rows 5 and 6 (see Fig. 2B). Both structural observations indicate PS of photoreceptors within row 2D. This is the only MB 1-4 row where four cells are present in the distal tier, suggesting a potential functional difference.
Spectral sensitivity
Photoreceptors of the dorsal and the ventral hemispheres produced broad
spectral sensitivity curves with peak sensitivities between 450 nm and 550 nm.
Although the averaged spectral sensitivity curves of dorsal and ventral
hemisphere photoreceptors peak at different wavelengths, they cover the same
spectral range with a similar sensitivity distribution and they are therefore
considered to be identical (Fig.
6A,B). In contrast, the photoreceptors of rows 5 and 6 produced
narrow spectral sensitivity curves (<100 nm bandwidth), peaking at
565±5 nm (N=8, 2 stained -
Fig. 6D). The photoreceptors
within row 2D also had narrow spectral sensitivity curves peaking at
566±4 nm (N=6, 3 stained -
Fig. 6C). Row 2D and row 5 and
6 receptors are therefore not only very similar in their polarization
sensitivities, but also almost identical in their spectral sensitivities.
Their narrow spectral sensitivity curves resemble the narrowly tuned
sensitivity curves of colour receptors.
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Directions of maximal sensitivity to the e-vector of polarized light (max)
Not surprisingly, the polarization orientations to which photoreceptors
were the most sensitive differed by 90° from the orientations to which
they were the least sensitive (Fig.
3A,B, Table 1). On
the basis of anatomical studies, Marshall et al.
(Marshall et al., 1991a)
proposed that Gonodactylus chiragra possesses four groups of
photoreceptors with unidirectional microvilli oriented at +45°, -45°,
90° and 0°. If this hypothesis is right, four max
values should be found amongst the polarization-sensitive photoreceptors.
Indeed, the electrophysiologically measured max values fall
clearly into four groups within ± 5° of the expected
max directions (Table
1). Staining of the photoreceptors after recordings confirmed the
predictions of Marshall et al. (Marshall
et al., 1991a) that each rhabom contains two populations of cells,
Group I and Group II receptors, with mutually perpendicular
max values (Fig.
4D). Within the type I rhabdoms of the hemispheres and rows 5 and
6, Group I is formed by three photoreceptors (R1, R4, R5) and Group II by four
photoreceptors (R2, R3, R6, R7) (Fig.
2A). The situation in the type II rhabdom of row 2D is, however,
different in that the rhabdom consists of only four photoreceptors R2, R3, R6
and R7 (Fig. 2B). However,
these receptors are also divided into two groups, R2, R6 and R3, R7, which are
sensitive to orthogonal e-vector directions of light
(Fig. 4C,D,
Table 1). All `high PS cells'
within rows 2D, 5 and 6 and the receptors of the dorsal hemisphere were
sensitive to an e-vector of either +45° or -45° relative to the
equatorial MB (Table 1). The
receptors of the ventral hemisphere were maximally sensitive to an e-vector
orientation of 0° or 90°, respectively. Thus, together, the
stomatopod's hemispheres sample four directions of polarized light: +45°,
-45°, 0° and 90° (Table
1).
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Discussion |
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Within the structurally unspecialized hemispheric retina, the mean PS
values of the photoreceptors R1-R7 (PS=3.8±1.6) are similar to values
that have been reported for photoreceptors of the crayfish and the green crab
(Glantz, 1996a;
Glantz, 1996b;
Shaw, 1966;
Shaw, 1969;
Waterman and Fernandez, 1970).
The mean PS value of the stomatopod's `high PS receptors' is significantly
increased (PS=6.1±2). In rows 5 and 6 this may be attributed to the
strictly aligned and regularly layered microvilli
(Marshall et al., 1991a;
Snyder, 1973;
Stowe, 1983). Other factors
such as fixed orientation of the rhodopsin and its aldehyde group within the
microvillus may also play a role but we have no evidence for this. Less
expected was the high PS value in photoreceptors of row 2D, because it was
believed that all photoreceptors of rows 1-4 are involved in polychromatic
colour vision (Cronin and Marshall,
1989b; Marshall et al.,
1991b). Confusion is likely to occur between colour and
polarization information, and therefore many animals [an exception is the
butterfly (Kelber et al.,
2001)] structurally destroy PS within their colour receptors
(Wehner and Bernard, 1993).
Marshall et al. (Marshall et al.,
1991a) described orthogonal arrays of microvilli within individual
receptors of rows 1-4. Furthermore it was shown that the thickness of the
orthogonal microvillar layers often varied greatly within these rhabdoms. Both
of these morphologies theoretically decrease PS remarkably. Our
electrophysiological recordings confirmed these anatomical predictions for the
colour receptors (rows 1, 3, 4 and 2P), which did not show appreciable
sensitivities to linearly polarized light (2.3±1). However, row 2D was
an exception. Re-examination of the ultrastructure of the row 2D rhabdom
revealed that single photoreceptors here also possess unidirectional
microvilli, which renders them sensitive to linear polarized light. The
rhabdom 2D also consists of regular layers of orthogonal microvilli of
identical thickness, albeit they are three times thicker than in rows 5 and 6,
which may decrease PS due to self-screening (see
Fig. 2B). It cannot be
determined from our studies if the low PS in 2P receptors is solely due to the
structure of the individual receptors or to the filter effect of the distally
situated `high PS receptors' within row 2D, which filter out two orthogonal
e-vector directions of linearly polarized light (+45°, -45°).
Spectral sensitivity of `high PS cells'
Spectral sensitivity measurements revealed that all `high PS cells' had
similar narrow spectral sensitivity curves (bandwidth <100 nm) peaking at
565±5 nm (Fig. 6C,D).
The R1-R7 cells throughout the retina of crayfish are also sensitive to
`yellow' light, peaking at 561 nm
(Waterman and Fernandez,
1970), although their spectral sensitivity curves are broader than
those of the stomatopod's `high PS cells'. The narrow spectral sensitivity
curves of `high PS cells' differ from previous microspectrophotometric
measurements, where broad spectral absorption spectra were estimated for a
variety of gonodactyloid species (Cronin et
al., 2002; Cronin and Marshall,
1989a; Cronin et al.,
1994a). Electrophysiological measurements are performed on the
intact eye, so that filtering effects of all the overlying optical structures
are taken into account, whereas microspectrophotometric measurements are from
absorbance of excised photoreceptor parts and the estimated spectral
sensitivity is based on the photoreceptor and filter lengths alone. Narrow
spectral sensitivities have been predicted for row 2D receptors, because of
the presence of an intrarhabdomal filter between R8 and row 2D (see
Fig. 2)
(Marshall et al., 1991b). No
such filters have been described for rows 5 and 6 and the narrow spectral
sensitivity curves measured electrophysiologically are a surprise especially
in view of the long lengths of the rhabdoms (over 100 µm). However, it is
possible that filtering effects at the level of the R8 cell, the cornea or the
crystalline cones exist here.
There are possible reasons for `high PS cells' to be sensitive to yellow
light. Water over reefs transmits light best around 550 nm
(Jerlov, 1976), which argues
for a sensitivity match of the `high PS cells' to the environmental stimulus
conditions. Furthermore, the degree to which light is polarized in water is
wavelength dependent with a minimum at 450-500 nm
(Cronin and Shashar, 2001;
Ivanoff and Waterman, 1958;
Jerlov, 1976;
Shashar et al., 2004). It is
therefore useful to position the spectral peaks of polarization receptors on
either side of this polarization minimum.
Polarization processing
In general, decapod crustacean rhabdoms possess two groups of polarization
receptors sensitive to orthogonal directions of polarized light, which provide
separate pathways to the lamina, the first optic ganglion beneath the retina
(Eguchi, 1965;
Shaw, 1966;
Waterman and Fernandez, 1970).
Such a dual channel pathway may also exist in Gonodactylus chiragra.
The determination of max revealed two populations of
polarization-sensitive cells within each rhabdom. For clarity we will describe
the findings for rows 5 and 6, row 2D and for the hemispheres separately.
In rows 5 and 6 the two populations of polarization-sensitive cells within
each rhabdom coincide with the two morphological groupings (Group I and Group
II) within the R1-R7 cells. max was found to be at -45°
and +45°, respectively. The information from each retinula cell group is
directed into two separate lamina layers
(Kleinlogel and Marshall,
2005; Kleinlogel et al.,
2003). Thus separate information channels may exist for linearly
polarized light at +45° and -45° with possible antagonistic input to
polarization-sensitive interneurons in the medulla.
In contrast, in row 2D the two populations of polarization sensitive cells
consist of only two cells each, which belong to the same cell group amongst
the R1-R7 cells; R2, R6 and R3, R7. In a right eye, max for R2
and R6 is at +45° and max for R3 and R7 is at -45°
(Fig. 4D,
Table 1). Owing to the fact
that the retinula cell arrangement in 2D is symmetrical
(Fig. 4C), we currently assume
that orthogonal PS information either cancels out within this tier or that it
is retained between R2 and R6 versus R3 and R7. Two bits of evidence
suggest the former is more likely. Firstly, the four photoreceptor axons
originating in row 2D all terminate in the same lamina layer and separation of
the two orthogonal polarization channels into, for example two sub layers, has
not been shown here (Kleinlogel and
Marshall, 2005). Secondly, row 2D fits into the scheme of colour
sensitivity within stomatopod vision
(Cronin and Marshall, 1989a;
Cronin and Marshall, 1989b) and
high polarization sensitivity within colour receptors is not desirable because
of possible confusion of colour with polarization information
(Wehner and Bernard, 1993).
Clearly we need to know more about the information processing beneath the
retina before too much further discussion.
It is worth mentioning that the retinal design of row 2 ommatidia differs
from rows 1, 3 and 4 ommatidia in the sense that the cell groups forming the
two retinal tiers are inverted (Marshall
et al., 1991a). This cell inversion has no direct effect on the
subretinal wiring of photoreceptor axons
(Kleinlogel and Marshall,
2005; Kleinlogel et al.,
2003), nonetheless, the structural differences may indicate a
different function of row 2D beyond the `colour vision system'. Since all
`high PS cells' are homochromatic, rows 2D, 5 and 6 receptors could
potentially subserve the same polarization system without confusing
polarization with colour information
(Wehner and Bernard,
1993).
Another retinal modification is found in rows 5 and 6. The photoreceptor
arrangement in the retina of row 6 is rotated 90° counter-clockwise in
relation to row 5 (in a right eye), so that each cell group in row 6 produces
microvilli arranged perpendicularly to the ones produced by the same cell
group in row 5 (Fig. 4D). Thus
the same cell groups of the two rows are sensitive to orthogonal e-vector
orientations (Marshall et al.,
1991a), but terminate in the identical lamina plexiform layer
(Kleinlogel et al., 2003).
Here again knowledge of the neural connectivity of photoreceptors is
indispensable for interpretation of the above observations with regard to the
putative polarization system.
In the dorsal and ventral hemispheres the two populations of
polarization-sensitive cells within each rhabdom also coincide with the two
morphological groupings (Group I and Group II) within the R1-R7 cells. In the
dorsal hemisphere, max was found to be at -45° and
+45°, respectively, whereas in the ventral hemisphere max
was at 0° and 90°, respectively
(Table 1). In contrast to other
crustaceans examined to date, the retinula cell arrangement in one hemisphere
of the eye of Gonodactylus chiragra is rotated 45° relative to
the other (Marshall et al.,
1991a). Consequently the R1-R7 cells within the hemispheric
retinas of Gonodactylus chiragra sample together four e-vector
orientations of polarized light. Most of the ommatidia of the ventral and
dorsal hemispheres view the same portion of the visual field and they could
therefore provide four information channels for polarized light simultaneously
(Marshall and Land, 1993).
This would theoretically eliminate neutral points at ±45° inherent
to a two-dimensional polarization analyser system
(Bernard and Wehner, 1977).
However, we consider the integration of the polarization channels from the two
hemispheres at an early stage of visual processing rather unlikely. This is
because the first three visual neuropiles, like the retina, are divided into
three areas, one under each hemisphere and one under the MB, which suggests
that visual information from the two hemispheres remains isolated and is
processed separately (Kleinlogel and
Marshall, 2005; Kleinlogel et
al., 2003).
Biological significance of polarization vision
The `high PS cells' within the stomatopod's retina form a linear array of
mutually perpendicular e-vector analysers, all of which examine a narrow
equatorial strip of the visual scene of 10° diameter
(Marshall and Land, 1993).
Stomatopods employ vertical scanning eye movements to sweep their linear array
of MB receptors over objects of interest. It is believed that these unorthodox
eye movements serve the sequential acquisition of colour and polarization
information by the specialized MB receptors
(Land et al., 1990). They have
rotational eye movements too (Land et al.,
1990) so that in fact PS relative to the outside world changes
continuously. This could potentially remove the ambiguity inherent in having
only two preferred e-vector sensitivities
(Bernard and Wehner, 1977).
Octopus can discriminate e-vector angular differences as low as 20° within
a single target and this is possibly facilitated by head or eye movements
(Shashar and Cronin,
1996).
Polarization vision under water clearly provides advantages such as
contrast enhancement in the scattering environment
(Lythgoe, 1971;
Lythgoe and Hemmings, 1967;
Nilsson, 1996), camouflage
breaking of polarization reflective prey
(Bernard and Wehner, 1977;
Shashar et al., 2000;
Shashar et al., 1998) and
orientation and navigation in the polarized-light field
(Waterman, 1981;
Wehner, 2001). Many
gonodactyloid stomatopod species, but not Gonodactylus chiragra,
possess polarization-specific body markings and they may use their `high PS
cells' to recognize these remarkable signals displayed by conspecifics in
aggressive and mating behaviour (Cronin et
al., 2004; Cronin et al.,
2003). The use of polarization signals in water is advantageous
compared to colour signals because the colour of objects changes with depth as
a result of the varying attenuation across the spectrum, but patterns caused
by changes in reflected polarization remain constant
(Tyler, 1963;
Waterman, 1955). Polarimetric
measurements have shown that stomatopod cuticle strongly reflects polarized
light in the same waveband that `high PS cells' are sensitive to
(Cronin et al., 2003).
Moreover, stomatopod cuticle is strongly polarized (50%-70%) compared to the
background polarization (30%-50%) and therefore stands out
(Cronin et al., 2003). The
degree of polarization decreases in water exponentially as a function of
distance. Polarization vision is therefore particularly useful for short-range
visual tasks, such as communication, without attracting unwanted attention
from distant observers (Shashar et al.,
2004).
Gonodactylus chiragra is rather exceptional as this species lacks
coloured and polarized body markings. They are one of the most restricted
species in habitat type, and competition for suitable cavities is therefore
intense. It appears that the evolution of lethal weapons for escalated combat
rather than body signals for ritualized fighting was more suitable for this
species (Caldwell and Dingle,
1976).
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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