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First published online April 18, 2008
Journal of Experimental Biology 211, 1376-1385 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015941
Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Oncorhynchus mykiss)
1 Department of Biology, University of Victoria, PO Box 3020 STN CSC, Victoria,
British Columbia, V8W 3N5, Canada
2 Retinal Signal Processing Group, Netherlands Institute for Neuroscience,
Meibergdreef 47, 1105 BA Amsterdam, The Netherlands
3 Department of Neurogenetics, Academic Medical Center, University of Amsterdam,
Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
* Author for correspondence at present address: Department of Biology, Center for Neuroscience Studies, Queen's University, Kingston, Ontario, K7L 3N6, Canada (e-mail: craig.hawryshyn{at}queensu.ca)
Accepted 19 February 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: ultraviolet, polarization sensitivity, electrophysiology, fish, cobalt, horizontal cell, electroretinogram, compound action potential
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Parkyn et al., 2003;
Novales Flamarique and Hawryshyn,
1997; McFarland and Munz,
1975a; Pomozi et al.,
2001). The complexity of the underwater photic environment is
mirrored by the diversity of visual adaptations that have evolved to perceive
these qualities of light (Barry and
Hawryshyn, 1999; McFarland and
Munz, 1975b; Novales
Flamarique and Hawryshyn, 1993). Many species of fish have evolved
visual mechanisms for the perception of linearly polarized light and
behaviours based on this perception, such as spatial orientation behaviour for
either laboratory or natural illumination experiments
(Hawryshyn and McFarland,
1987; Hawryshyn et al.,
2003; Parkyn and Hawryshyn,
2000; Parkyn et al.,
2003; Mussi et al.,
2005; Shashar and Cronin,
1996; Shashar et al.,
1998; Shashar et al.,
2001; Shashar and Hanlon,
1997; Waterman and Hashimoto,
1974).
Biophysical models have been proposed to explain the selective absorption
of electric-vector (e-vector) orientations of polarized light in vertebrate
photoreceptors (Novales Flamarique et al.,
1998; Roberts et al.,
2004; Roberts and Needham,
2007). The proposed models for e-vector absorption include: (i)
internal reflection within double cones onto neighbouring
ultraviolet-sensitive (UVS) cones resulting from the partitioning membrane and
the geometry of the cone mosaic (Novales
Flamarique et al., 1998;
Allison et al., 2003); (ii)
axial dichroism of cone photoreceptors through tilting of the outer segment
disc membranes (Roberts et al.,
2004; Roberts and Needham,
2007).
A number of techniques have been used to examine polarization sensitivity
(PS) in several teleost species including: heart rate conditioning
(Hawryshyn and McFarland,
1987), single unit recording from the torus semicircularis
(Coughlin and Hawryshyn, 1995)
and the optic tectum (Waterman and
Hashimoto, 1974), compound action potential (CAP) recordings from
the optic nerve (Parkyn and Hawryshyn,
1993; Parkyn and Hawryshyn,
2000), electroretinograms (ERGs)
(Hawryshyn et al., 2003) and
behavioural orientation and discrimination paradigms
(Hawryshyn et al., 1990;
Parkyn et al., 2003;
Degner and Hawryshyn, 2001;
Mussi et al., 2005). However,
examinations of the neuronal pathways underlying PS have been restricted to
several species of cyprinids and salmonids. These studies have mainly employed
techniques such as single unit recording techniques in the torus
semicircularis and CAP recording techniques in the optic nerve (for a review,
see Hawryshyn, 2000).
CAP recordings by Parkyn and Hawryshyn
(Parkyn and Hawryshyn, 1993;
Parkyn and Hawryshyn, 2000)
identified horizontal and vertical polarization detector mechanisms by
examining the PS of the four cone mechanisms isolated through chromatic
adaptation. Chromatic adaptation is a technique that uses spectral backgrounds
to selectively depress cone mechanisms, usually resulting in the isolation of
one cone mechanism's sensitivity [see Hawryshyn and McFarland
(Hawryshyn and McFarland,
1987) for an illustration of this technique]. Briefly, these
experiments, like those performed on goldfish
(Hawryshyn and McFarland,
1987), demonstrated that the UVS cone mechanism mediated vertical
PS, whereas the medium and long wavelength-sensitive (MWS and LWS) cone
mechanisms mediated horizontal PS. When a spectrally broad background is used
in conjunction with UV linearly polarized stimuli, PS curves show a `W-shaped'
PS function. Peak PS occurs at 0° and 90°, representing the combined
presence of the vertical and horizontal polarization detector mechanisms. A
full description of these observations is provided in Parkyn and Hawryshyn
(Parkyn and Hawryshyn, 1993)
and Coughlin and Hawryshyn (Coughlin and
Hawryshyn, 1995). In a recent study, we examined PS of three
species of damselfishes (three-spot damselfish, Dascyllus
trimaculatus; blacktail damselfish, D. melanurus and blue-green
chromis, Chromis viridis) using ERG recordings
(Hawryshyn et al., 2003). The
non-invasive nature of the technique made it an attractive methodology for
measuring PS and doing so repeatedly in the same individual. The observed PS
from ERG recordings was more complex (four peaks) than the two-channel
W-function commonly found in salmonids using CAP recording. ERG evaluation of
PS in salmonids had not been previously attempted. Studies that have used ERG
recording to measure PS in vertebrates such as pigeons have resulted in
conflicting results, largely because of methodological issues such as avoiding
the measurement of UV polarization sensitivity and because of incorrect
interpretation of ERG data (Kreithen and
Keeton, 1974; Delius et al.,
1976; Hzn et al.,
1995).
The overall purpose of the work presented here was to explore where in the retina critical coding steps may occur for polarization vision. The sensitivity to polarized light was determined at two locations: (1) at the output stage of the retina, by recording CAPs in the optic nerve (late stage processing), and (2) at the input stage of the retina, by recording the ERG (early stage processing). Using chromatic adapting backgrounds, the spectral sensitivity of the various components of the responses was determined and using a pharmacological approach, the nature of the underlying neuronal mechanism was studied. Here we show that critical polarization processing takes place in both the outer and inner retina. Short and long wavelength chromatic adaptation predictably displaced the angular position of the intermediary peaks in ERG PS curves relative to the peak vertical and horizontal detector mechanisms by changing the weighting of opponent interactions. Cobalt injections, which are known to block feedback of horizontal cells on cones, resulted in an elimination of the intermediary peaks in ERG PS curves. The presence of these intermediary peaks in ERG PS curves and their absence in CAP PS strongly implicates a special role of the outer retina in processing linearly polarized light.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Parkyn and Hawryshyn,
2000). The photic conditions within the holding facility were
provided by full spectrum fluorescent lamps (6500 K). All experimental
procedures and animal care were approved by the University of Victoria Animal
Care Committee, under the auspices of the Canadian Council for Animal
Care.
Preparation of fish
Experimental preparations for both electroretinograms (ERGs) and compound
action potential (CAP) recordings are described elsewhere in detail
(Beaudet et al., 1993;
Hawryshyn et al., 2003;
Parkyn and Hawryshyn, 2000).
In brief, rainbow trout were immersed in a solution of 125 mg
l–1 tricane methanesulphonate (MS-222) until the fish reached
stage IV anaesthesia (Joly et al.,
1972). Standard length (cm) and body mass (g) were measured.
Subcuteaneous injections of a general anaesthetic, Maranil (0.005 mg
kg–1 body mass) and an immobilizing agent, pancuronium
bromide (0.05 mg g–1 body mass) were administered at several
sites. The test fish were then placed in a holding cradle in a Faraday cage.
Experimental fish were irrigated with aerated fresh water (10°C, flow rate
of approximately 3 ml s–1) and the body covered with a moist
cloth. For CAP experiments, the dermis overlying the right frontal bone was
removed with a scalpel and surgical drill, holding a dental burr. This
provided access to the right rostral optic tectum through which the recording
electrode was advanced into the optic nerve.
Experimental apparatus
The optical system and recording apparatus have been described previously
(Hawryshyn et al., 2003;
Parkyn and Hawryshyn, 2000).
Two background channels using 250 W quartz-halogen lamps (Ushio Cypress, CA,
USA) were used to provide constant background fields and chromatic adaptation.
Long and short wavelength cut-off interference filters, Schott colour filters
and neutral density filters/wedge, were used to manipulate both the energy and
wavelength distribution of each background channel. A quantum catch model was
employed to determine filter combinations necessary to produce the desired
background conditions (Table
1). A bifurcated fibre optic (fused silica, n.a.=0.22; Fiberoptic
Systems Inc., Simi Valley, CA, USA) was used to superimpose the background
channels onto the eye. The stimulus channel used a 300 W xenon arc lamp system
(Thermo Oriel, Stratford, CT, USA). The optical path consisted of a
monochrometer (Instruments SA), Inconel quartz neutral density wedge
(0–4.0 neutral density; Melles-Griot, Rochester, NY, USA), shutter
(Uniblitz, Vincent Associates, Rochester, NY, USA), optical filters to block
spectral sidebands, and UV optics to match the numerical aperture of the
liquid light pipe (n.a.=0.74). The stimulus and background illuminated the
left eye of the fish. Both the stimulus and background fields were spatially
broad, to mimic natural presentation of celestial and underwater-polarized
light. Spectral sensitivity was measured in 20 nm increments, from 360 to 620
nm, using a staggered wavelength presentation to prevent adaptation to a
certain region of the spectrum.
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For PS measurements, a UV-transmissive linear polarizer (HNP'B, Polaroid
Corporation, Concord, MA, USA; manually adjusted) was placed over the ferrule
of the liquid light pipe. Measurements were randomized, from 0° to
180°, in 15° increments, where the 0°/180° e-vector axis was
defined as vertical relative to the gravitational axis of the fish and
90/270° was defined as horizontal
(Hawryshyn and McFarland,
1987). Fish were light adapted with unpolarized light from the
background channels, and a plane-polarized, 360 nm stimuli, in 0.2 log unit
increment steps, was used to measure UV PS. The use of two light pipes, one
for the stimulus and the other for the background eliminated e-vector
adaptation from the background channel. A quantum catch model was used to
generate photic conditions aimed at carefully controlling the level of light
adaptation of the respective cone mechanisms:
 | (1) |
) denotes the visual pigment absorption
coefficient of receptor (i), a G() denotes the photon
irradiance (spectral energy distribution) of the background light field and
d() denotes wavelength (nm). Integrations were performed for
each receptor mechanism, between 300 and 800 nm, for the various background
conditions considered. This assessment, in addition to cone mechanism light
adaptation dynamics (Hawryshyn,
1991), allowed us to finely control the state of adaptation of the
cone mechanisms. Such considerations were essential to avoid complete
suppression of either the UVS or LWS cone mechanisms. The following background
adaptation conditions were used: (i) white light background – 700 nm
short pass (SP; Coherent Inc., Santa Clara, CA, USA; also used in ii and iii)
plus 2.0 neutral density filters (Coherent Inc.; also used in ii and iii) in
each background channel (1 and 2); (ii) LWS cone mechanism adaptation –
600 nm long pass (LP; Coherent Inc.; cut-off filter) and 1.5 neutral density
in channel 1, and 700 nm SP and 2.0 neutral density filters in background
channel 2; (iii) UVS cone mechanism adaptation – UG-11 (Shott filter)
and 1.3 neutral density filters in channel 1, and 700 nm SP and 2.0 neutral
density filters in channel 2. Spectral energy distribution curves are shown in
Fig. 1.
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;
Vigh and Witkovsky, 1999) and
in fish (Fahrenfort et al.,
2004). Injections of either cobalt chloride (Sigma-Aldrich) or
saline were made at the limbus of the left eye using a 30-gauge needle. Final
concentrations of cobalt were estimated following the method used by Demarco
and Powers (Demarco and Powers,
1989). In short, the average volume of the vitreous was estimated
to be 145 µl, and 10 µl of 4.26 mmol l–1 cobalt was
injected, resulting in an estimated final ocular concentration of 0.275 mmol
l–1. These concentrations represent first order
approximations of the cobalt chloride concentration in the eye. These values
may not reflect what is actually present in the outer retina at the time of
our measurements (i.e. these values are likely overestimates). For instance,
our estimates of the concentration of cobalt chloride may not be directly
comparable to those in an isolated retina or eyecup preparations superfused
with physiological medium and pulsed with cobalt chloride.
Recording procedure: electroretinogram (ERG)
A glass electrode [1 mm i.d., loaded with saline (28 p.p.t. sodium
chloride)] was inserted into a saline filled half-cell (A-M systems Inc.,
Carlsborg, WA, USA), and the tip was positioned using a micromanipulator on
the dorsal-nasal surface of the left eye. A ground electrode was attached to
the caudal fin and a chlorided-silver reference electrode was placed in the
right nares of the test fish. Fish were acclimated for 45 min prior to
experiments using chromatic adaptation or cobalt treatments. A Grass Hi-Z
probe (Grass-Telefactor probe, Grass Instruments, West Warwick, RI, USA)
provided the input to a Grass instruments P-5 preamplifier (bandpass filter
settings, 0.3 Hz low-pass and 300 Hz high-pass). The amplified signal was
analyzed with a 16-bit A/D data acquisition board (National Instruments, Inc.,
Austin, TX, USA). A custom-designed software analysis module determined the
b-wave amplitude by measuring the change in potential from the peak a-wave to
peak b-wave, during the period 150 ms post stimulus onset. The stimulus
duration was 500 ms with an inter-stimulus interval of 20 s.
Compound action potential (CAP)
A sharpened Teflon-coated chlorided-silver electrode (0.5 mm diameter, 0.5
mm exposed tip) was inserted into the optic nerve of the left eye using a
micromanipulator, following procedures used by Parkyn and Hawryshyn
(Parkyn and Hawryshyn, 1993;
Parkyn and Hawryshyn, 2000).
Correct placement of the recording electrode into the optic nerve was crucial,
since Coughlin and Hawryshyn (Coughlin and
Hawryshyn, 1995) demonstrated that optic tecta do not possess UV
polarization-sensitive neurons. To avoid misplacement of the recording
electrode, a custom-designed stereotaxic apparatus was used. Further, the
waveform recorded in response to photic stimuli differs between tectal and
optic nerve location of the electrode tip (see
Parkyn and Hawryshyn, 2000).
Post mortem dissections verified the correct trajectory and placement
of the electrode. Ground and reference electrodes were placed on the fish as
described above.
The amplitude of the onset response of the optic nerve compound action potential was determined by comparing the baseline noise amplitude 50 ms prior to stimulus onset with the response amplitude 50 ms post stimulus onset.
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The model
The input signals for the model are described by Eqn
(2) and
(3) and were taken as the
logarithmic response of polarization amplitude detected:
 | (2) |
 | (3) |
is the polarization angle of the
incident light. A linear subtractive model was used to examine the opponent
interactions between the V and H polarization detector
mechanisms:
 | (4) |
 | (5) |
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Optic nerve recording waveforms exhibited responses at light onset and offset.
The onset response amplitudes were plotted against stimulus intensity to
illustrate the response dynamics of ganglion cell axons in the optic nerve.
The response versus intensity curve shown in
Fig. 2C was described by a
third order polynomial expression. Threshold intensity was estimated using a
criterion response set at 50 µV above baseline and interpolating the
stimulus intensity. The ERG recordings shown in
Fig. 2B share the same
graphical format as Fig. 2A. At
higher intensities, the control ERG waveforms show the classical components
[a-, b-, c- and d-waves (Brown,
1968)]. The intensity response relationship is given in
Fig. 2D with the dashed line
representing a third order polynomial fit. For these recordings the threshold
criterion was set at an amplitude of 20 µV above baseline.
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Next we examined the effect of these adapting backgrounds on PS. If we compare UV PS for CAP and ERG recording techniques, the CAP response has its characteristic W-shape whereas the ERG has intermediate peaks at 45° and 135° (Fig. 4). The peaks for the ERG are all equally sized. Although a small secondary peak at 135° could also be seen in the CAP response, the secondary peaks are a prominent feature of the ERG and very minor in the CAP. Since the CAP response has been described in detail elsewhere, we will focus for the rest of the paper on the ERG responses. The model was fit to all polarization tuning curves. The open squares represent the model fit for the vertical system (SV) and the open diamond symbols represent the horizontal system (SH). Similar model traces are shown in Fig. 5A,B. The model fits show that chromatic adaptation influences the breadth or angular bandwidth of both the vertical and horizontal detector mechanisms. When a longwave background (600 nm longpass) was used the horizontal detector mechanism narrowed and the vertical mechanism broadened. The opposite was observed when a UV background (UG-11) was used.
Previously, we determined that the vertical polarization detector was dominated by the UVS cone mechanism, whereas the horizontal polarization detector was dominated by the LWS cone mechanism. If the intermediate peaks were due to an opponent interaction between these two polarization mechanisms, chromatic adaptation would lead to a shift of the intermediate peak away from the more sensitive cone mechanism or polarization detector. This prediction was confirmed in Fig. 5A. Under 600 LP chromatic adaptation, the peak of the ERG profile shifted from 45° and 135° (Fig. 4A) to 60 and 120°, respectively. Similarly, chromatic adaptation with UG-11 (UV chromatic adaptation) shifts the peaks in the opposite direction towards the vertical detector mechanism (Fig. 5B).
Next the site of this inhibition was studied. Sub-milimolar concentrations of Co2+ are known to inhibit feedback from horizontal cells to cones. An intraocular injection of 0.275 mmol l–1 Co2+ yields a similar concentration. First, the sensitivity of the ERG responses to Co2+ was determined. Fig. 6A shows the ERG response for various stimulus intensities. The ERG response shape changed after application of cobalt (Fig. 6B). The A-wave was reduced and the B-wave was temporally broader. However, the intensity response relationship did not change appreciably (Fig. 6C), indicating that the sensitivity of the cones was not affected.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Origin of Intermediary peaks: cobalt treatment and intermediary peaks
Our study revealed significant differences in the ERG waveform
characteristics of control and cobalt chloride-treated test fish. For
instance, the A-wave component was diminished in cobalt-treated fish in
relation to the control. Recent studies have shown that cobalt treatment can
block inward currents in rod photoreceptors, resulting in a suppression of
signal transmission (Green and
Kapousta-Bruneau, 1999; Yuan
and Yang, 1997). Yuan and Yang
(Yuan and Yang, 1997) suggest
that cobalt-induced signal suppression results from a blockage of glutamate
uptake by photoreceptors.
Cobalt is known to block horizontal cell-mediated feedback on cones in
goldfish retina (Fahrenfort et al.,
2004; Thoreson and Burkhardt,
1990). The result of blocking negative feedback of horizontal
cells on cones is that the cone synapse is rendered out of its working range
(Kamermans et al., 1998;
Kamermans et al., 2001).
Furthermore, blocking feedback of horizontal cells on cones will lead to a
reduction of the high pass filter characteristics of the synapse. Consistent
with this we observed a lower amplitude signal with a temporally broader
B-wave. The broader B-wave suggests that blocking horizontal cell feedback
with Co2+ treatment eliminates the high pass filtering
characteristic of feedback. Cobalt treatment may have had other effects on the
system. For instance, Co2+ could have an effect on cellular
shutdown mechanisms in photoreceptors (e.g. arrestin and/or guanylyl cyclase)
or as a recent study has shown, Co2+ could cause the production of
hypoxia-induced factor-1 alpha in retinal pigment epithelial cells
(Wang et al., 2005). This
possibility would be comparable to mimicking hypoxic conditions in the retinal
pigment epithelium, thus suppressing the C-wave. However, the finding that the
D-wave component had reduced amplitude and a temporally broader response
strongly suggests that Co2+ reduced horizontal feedback. Thus, the
implications of these other cobalt effects for our study would seem to be
rather limited.
As discussed previously, sub-millimolar concentrations of Co2+ inhibit feedback from horizontal cells to cones. Intraocular concentrations of 0.275 mmol l–1 Co2+ resulted in significant attenuation or elimination of the intermediary peaks. The intermediary peaks appear to function as feedback activity, and that significant reduction in horizontal cell feedback results in the two channels being expressed primarily in the feed-forward pathways.
To support the hypothesis that the intermediary peaks are the result of feedback of horizontal cells on cones, we need to identify a feed-forward signal that generates the ON-bipolar response that is reduced when feedback is reduced. Our results suggest that such a reduction in feed-forward signals occurs in both the chromatic adaptation conditions and the Co2+ treatments. During the UVS cone adaptation and Co2+ treatments, there is a relative reduction in the UVS cone mechanism feed-forward signal due to the reduction in feedback of horizontal cells onto the LWS/horizontal detector. The LWS cone mechanism adaptation condition resulted in a relative reduction in inhibitory feedback onto the UVS cones, resulting in a relatively smaller feed-forward signal from the LWS/horizontal detector mechanism compared to the other conditions.
Potential mechanisms for the generation of intermediary peaks
UV polarization vision in teleosts is dependent on the presence of two
differentially sensitive polarization detectors. These detectors are
represented by different spectral classes of cones in the case of rainbow
trout: the vertical detector mediated by the UVS cones and the horizontal
detector by the MWS/LWS double cones. How are the intermediary peaks
generated?
First, we need to consider interactions between different spectral classes
of cones, for example, MWS/LWS members of double cones, and UVS/LWS cones
evident at the horizontal cell level and at higher levels in the visual
pathway of salmonid fishes (Coughlin and
Hawryshyn, 1995; Nakano et
al., 2006). Second, colour-coded neurons in the torus
semicircularis that show UV polarization sensitivity are always UV on/red off
(Coughlin and Hawryshyn, 1995).
Third, chromatic adaptation using a UV or a long wavelength background results
in changes in UV polarization sensitivity such as shifting the position of
intermediary peaks and increasing or decreasing the width of the horizontal
and vertical detector mechanism peaks.
It is clear from our experiments that cobalt blocks negative feedback of horizontal cells on cones, and that the modulation of polarization sensitivity comes principally through this feedback. The evidence from both the chromatic adaptation and cobalt treatment suggests that the outcome of the MWS/LWS opponent interaction (horizontal detector) influences the negative feedback of horizontal cells onto UVS cones and that UVS cones feedback to MWS/LWS cones through negative feedback from horizontal cells. At an e-vector orientation of 45° or 135°, the opponent interaction of MWS/LWS cones reduces the negative feedback on UVS cones, thus producing the intermediary peaks. Chromatic adaptation changes the balance of interaction between the vertical and horizontal detector mechanisms and thus if either detector dominates, it pushes the intermediary peak towards the depressed detector and it narrows the width of sensitivity of the depressed detector. The outcome of these interactions sets the output of the outer retina.
In addition, studies on turtle retina have shown that cone–cone
coupling can lead to the LWS cone mechanism providing excitatory input to
shortwave-sensitive cone mechanisms
(Itzhaki et al., 1992).
Cone–cone coupling could enhance sensitivity if two differentially
sensitive photoreceptor mechanisms were stimulated in a zone of overlapping
sensitivity [spectral or polarization
(O'Brien et al., 2004)].
Although this aspect of retinal function has not been examined for rainbow
trout, it could represent an additional mode of retinal processing in
polarization vision.
Work on insect polarization sensitivity suggests that antagonistic
interaction of polarization detectors, through opponency, has features
comparable to what we see in fish retina. Labhart and Meyer
(Labhart and Meyer, 2002)
suggest that POL neurons in the optic lobe of crickets receive input from
differentially sensitive polarization detectors that operate in an opponent
manner for purposes of signal conditioning. They indicate that polarization
opponency functions to enhance e-vector contrast for effective coding at low
degrees of polarization, and it moderates neuronal sensitivity to variations
in ambient intensity focusing activity on coding differential polarization
detector input.
Do spectral confounds interfere with polarization sensitivity?
Research to date indicates that spectral confounds are minimized by the
coincidence of spectral absorption of UVS and MWS/LWS cones in the UV portion
of the spectrum. Thus UV linearly polarized light stimulates the -band
absorption of the UVS cones and the β-band absorption of the MWS/LWS
cones, two orthogonally sensitive polarization detectors (see
Parkyn and Hawryshyn, 1993).
It is important to note, however, that the issue of spectral confounds
requires serious examination since stimulation of the MWS and/or LWS cone
mechanism could lead to a spectral signal of sufficient strength to confound
the polarization stimulus. However, our data argue strongly against this
possibility. (1) Recordings from retinal neurons (largely retinal ganglion
cells), performed to test for UV polarization sensitivity, always show
distinct vertical and horizontal polarization detector mechanisms
(Parkyn and Hawryshyn, 1993;
Parkyn and Hawryshyn, 2000). A
spectral confound would have the effect of showing either the horizontal
detector mechanism dominating the polarization sensitivity or polarization
sensitivity disappearing because the spectral signal becomes the salient
feature. (2) Test fish that have been shown to have UVS cone loss from the
central and ventral retina through programmed cell death
(Allison et al., 2003;
Allison et al., 2006), show
polarization sensitivity with only the horizontal detector mechanism present
(Hawryshyn, 2000). (3)
Recordings from neurons in the torus semicicularis (mid brain structure) show
similar characteristics of polarization sensitivity to retinal neurons
(Coughlin and Hawryshyn, 1995).
(4) Behavioural studies show that the UV content in linearly polarized stimuli
is essential for e-vector spatial orientation and e-vector discrimination
behaviour (Degner and Hawryshyn,
2001; Hawryshyn et al.,
1990; Mussi et al.,
2005; Parkyn et al.,
2003). If the UV spectrum is eliminated from the linearly
polarized stimulus with a UV cut-off filter or the UVS cones have disappeared
in the central and ventral retina, salmonid test fish are incapable of
responding to the polarization stimulus
(Hawryshyn at al., 1990;
Mussi et al., 2005). Spectral
confounds would distort or detrimentally affect e-vector spatial orientation
and discrimination.
So we conclude that spectral confounds play a relatively insignificant role in interfering with polarization sensitivity.
Behavioural relevance of feedback interactions in the retina
The current study on rainbow trout along with examination of damselfish
(green chromis) (Hawryshyn et al.,
2003) polarization sensitivity, indicate that these two species
have similar polarization processing in the outer retina. We have recently
used green chromis in behavioural studies examining polarization
discrimination. Green chromis appear to have very good polarization
discrimination capabilities; easily differentiating horizontal and vertical
planes of linearly polarized light independent of brightness
(Mussi et al., 2005). The
capacity for e-vector discrimination disappeared when the UV portion of the
light stimuli was filtered out, indicating that the presence of UV polarized
light is critical for e-vector discrimination. In addition, damselfish were
able to distinguish between relatively small e-vector orientations of
polarized light with the minimum separable e-vector of 15°–25°.
The discriminative performance of C. viridis was greatest at e-vector
orientations close to or at the point of maximum overlapping sensitivity of
the two polarization detector mechanisms. Thus polarization discrimination
appears to be at its optimal level of performance when the two detector
mechanisms are interacting through interneuronal processing mediated by
horizontal cells.
We have used rainbow trout in a related discrimination paradigm
(Degner and Hawryshyn, 2001). A
notable difference was that trout were not capable of polarization
discrimination on a horizontal line of sight. Rather trout could perform
discriminations on a downwelling projection of the polarization field. This
difference in polarization discriminative behaviour between species could be a
good indication of the functional utility of polarization vision in fishes.
Damselfish are strongly zooplanktivous, so one possible function of
polarization vision in damselfish could be the enhancement of contrast between
the zooplankter and background veiling radiance. In rainbow trout, however,
discriminative resolution of the e-vector is much poorer
(Degner and Hawryshyn, 2001)
and thus not as likely to be related to plankton feeding, but more likely to
be crucial for navigation (Parkyn et al.,
2003).
Despite the differences in functionality, negative feedback interactions between horizontal cells and cones modulates or shapes the feed forward polarization signal through the retina. The commonality seen in polarization sensitivity between species would suggest that this information processing is probably an important and general feature in polarization vision.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Allison, W. T., Dann, S. G., Helvik, J. V., Bradley, C., Moyer, H. D. and Hawryshyn, C. W. (2003). Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). J. Comp. Neurol. 461,294 -306.[CrossRef][Medline]
Allison, W. T., Dann, S. G., Veldhoen, K. M. and Hawryshyn, C. W. (2006). Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. J. Comp. Neurol. 499,702 -715.[CrossRef][Medline]
Barry, K. L. and Hawryshyn, C. W. (1999). Spectral sensitivity of the Hawaiian saddle wrasse, Thalassoma duperrey, and implications for visually mediated behaviour on coral reefs. Environ. Biol. Fishes 56,429 -442.[CrossRef]
Beaudet, L., Browman, H. I. and Hawryshyn, C. W. (1993). Optic-nerve response and retinal structure in rainbow-trout of different sizes. Vision Res. 33,1739 -1746.[CrossRef][Medline]
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0.275 mmol
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