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First published online May 18, 2006
Journal of Experimental Biology 209, 2034-2041 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02171
Spectral sensitivity of the two-spotted goby Gobiusculus flavescens (Fabricius): a physiological and behavioural study
1 Department of Biology, University of Bergen, PO Box 7800, N-5020 Bergen,
Norway
2 Division of Visual Science, Institute of Ophthalmology, University College
London, London, UK
* Author for correspondence (e-mail: anne.palm{at}bio.uib.no)
Accepted 14 February 2006
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maxat 508 nm) and the three cone
pigments (max 456, 531 and 553 nm). The cone population was
dominated by identical double cones containing the middle-wave-sensitive (MWS)
pigment, but with a small number of non-identical MWS/LWS
(long-wave-sensitive) and identical LWS double cones. Small populations of
large single cones also contained either the MWS or LWS pigment. The
short-wave-sensitive (SWS) pigment was found in small single cones. Lens
transmission was great reduced below 410 nm. The spectral sensitivity of the behaviourally determined reaction distance (RD) to prey at a high irradiance level 0.5 µmol m-2 s-1) correlated with the maximum sensitivity of the MWS cones, both peaking around 530 nm. However, at a lower irradiance level (0.015 µmol m-2 s-1)such a correlation was not so apparent. The RD was greatly reduced, though still maintaining a peak around 530-550 nm, but with a relatively smaller reduction in RD at shorter wavelengths. Optomotor behaviour displayed a somewhat similar spectral sensitivity to the RD responses at the higher light intensity. However, the peak was at slightly longer wavelengths at 550 nm, suggesting a greater input from LWS cones to the optomotor response.
Key words: visual pigment, reaction distance, optomotor response, Gobiusculus flavescens
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) or inferred
from electrophysiology (Parkyn and
Hawryshyn, 2000; Whitmore and
Bowmaker, 1989) and can give indications of spectral sensitivity
and the potential for colour vision (Barry
and Hawryshyn, 1999; Cameron,
2002). Histological studies can reveal the distribution of the
various photoreceptor classes (Reckel et
al., 2002; Van der Meer et
al., 1995), complementing the physiological measurements of
spectral sensitivity and providing estimations of visual acuity
(Fritsches et al., 2003;
Shand, 1997). However, none of
these methods can define visual performance, which can only be determined by
behavioural experiments (Douglas and
Hawryshyn, 1990; White et al.,
2004) involving either innate behaviours such as the optomotor
response (Krauss and Neumeyer,
2003; Schaerer and Neumeyer,
1996) or behavioural activities such as feeding strategies
(Job and Shand, 2001;
Utne-Palm, 2002). Correlations
of these methods of investigation can give insights into the retinal
mechanisms underlying visual performance, but can produce divergent results
(Neave, 1984;
Browman et al., 1990;
Miller et al., 1993;
Pankhurst et al., 1993;
Van der Meer, 1994;
Van der Meer, 1995). In the
present study of the two-spotted goby, Gobiusculus flavescens
(Fabricius), we have used microspectrophotometry (MSP) to determine the
complement of its visual pigments. In addition, behavioural studies were
carried out to investigate the visual ability of the goby, by studying its
reaction distance (RD) to prey and its optomotor response, under light
conditions that both matched and mismatched the peak sensitivities of its
visual pigments. The contributions of the different photoreceptor types to
prey or motion detection were studied by comparing the action spectra of the
RD and optomotor response studies with the spectral sensitivities of the
visual pigments.
Increasing illumination causes a significant increase in RD in G.
falvescens, with an asymptotic log-linear increase in RD with increasing
illumination (Utne, 1997).
Furthermore a change in wavelength composition seems to have the same
significant effect on RD as a change in illumination level
(Utne-Palm, 1999). G.
flavescens was found to have a significantly longer RD at 450-550 nm
compared to 630-730 nm or white light from a halogen source
(Utne-Palm, 1999), indicating
a higher sensitivity in the blue-green. Our predictions are that gobies will
be more sensitive to light that matches the peak absorbance of its visual
pigments than to light that falls between these maximum sensitivities. In
other words, RD will be longer and a small change in illumination level at the
peak absorbance will have a much greater effect on RD than the same change in
illumination at a wavelength away from the pigment maxima. Accordingly, we
predict that the optomotor response will persist at lower illumination levels
within wavelengths close to pigment maxima compared to wavelengths away from
the maxima. Furthermore, we predict that the relative numbers of the different
cone classes will have an effect, so that the dominant spectral class of cone
will have a positive effect on RD and optomotor response.
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; Hairston, Jr et al., 1982;
Breck and Gitter, 1983;
Walton et al., 1992) and can
also be sex dependent (Douglas and
Hawryshyn, 1990).
Microspectrophotometry
Retinas from ten gobies, five of each sex, were used in the MSP study. Fish
were dark adapted overnight, then sacrificed by cervical transection. All
procedures were carried out under dim red light. Eyes were enucleated,
hemisected and the anterior portion discarded. The retina was then separated
from the pigment epithelium and one or two small samples were prepared
immediately for measurement. The remaining tissue and the eyecup from the
other eye were lightly fixed in 2% glutaraldehyde solution for about 15-30 s,
washed in saline and then stored at 4°C in saline. Retinal samples from
this fixed tissue were used on subsequent days for up to 2 weeks after
preparation. Retinal samples were teased apart on a coverslip with razor
blades and the dispersed tissue mounted in saline containing 5% or 10%
dextran, then squashed with a second coverslip, which was sealed with wax.
Since MSP can only sample photoreceptors randomly, at least two pieces of
retina were analysed from different regions of each eye, in an attempt to
overcome any regional distribution of different classes of cone.
Microspectrophotometric recordings were made in the conventional manner
using a Liebman dual-beam microspectrophotometer
(Bowmaker et al., 1991;
Liebman and Entine, 1964;
Mollon et al., 1984). Spectra
were recorded at 2-nm intervals from 750 to 350 nm and from 351 to 749 nm on
the return scan. The outward and return scans were averaged. A baseline
spectrum was measured for each cell, with both beams in an unoccupied area
close to the cell, and this was subtracted from the intracellular scan to
derive the final spectrum. Two baseline scans were recorded for each cell and
averaged. All cells were fully bleached with white light and post-bleach
spectra recorded. The maximum absorption wavelength (max)
of both the absorbance spectra and difference spectra were determined by a
standard computer programme that best fits a visual pigment template to the
right hand limb of the spectra (Bowmaker et
al., 1991; Mollon et al.,
1984). Selection criteria were used to discard records that either
had low absorbance or were clearly distorted. In all cases, the spectra were
best fitted with a pure rhodopsin, vitamin A1-based template
(Govardovskii et al., 2000).
Three estimates of the max were made from the selected
records for each class of pigment; the max of the mean
absorbance spectrum, the max of the mean difference
spectrum and the mean of the max of the individual cells.
The max of the mean absorbance spectrum is taken as the
most reliable estimate of the peak sensitivity
(Mollon et al., 1984).
Lens transmission
The transmission spectra of the lenses from a single fish were recorded,
courtesy of R. H. Douglas (City University, London, UK). The lenses, about 1
mm in diameter, were mounted in a lens holder and spectra measured using a
Shimadzu-UV240 spectrophotometer fitted with an integrating sphere, as
detailed elsewhere (Douglas and McGuigan,
1989; Thorpe et al.,
1993).
Studies of behavioural visual capacity
About 200 wild-caught adult gobies were acclimatised in two 80 l aquaria
for at least 7 days, before being moved to the experimental aquarium. The
temperature was maintained at 8-10°C. Artificial white light was used
(Osram Lumilux de lux daylight LF 12-950, wavelength 400 to 750 nm), which
simulated (with exception of the UV part of the spectrum) the outside light
conditions of the actual time of the year, with full `daylight' (32 µmol
m-2 s-1) lasting for 10 h (autumn) to 8 h (winter), and
a daily dusk and dawn period of 45 min. All experiments began after 3 h of
full light and lasted for up to 3 h. Live copepods were offered daily.
Two different experimental paradigms were used to resolve the behavioural visual capacity of the goby: reaction distance (RD) to live prey, and the optomotor response. Both studies were preformed under different wavelengths conditions and illumination levels.
The light source used in the behavioural experiments was a 1000 W quartz
tungsten halogen lamp, with narrow band filters (half-bandwidth 10 nm) peaking
at 460, 510, 532, 550 and 560 nm, and a 660-nm cut-on filter. The peaks of
four of the narrow band filters (460, 510, 532 and 550 nm) matched the
max of the cones and rods of the goby, as determined by
MSP. The 560-nm narrow band filter, slightly offset from the
long-wave-sensitive (LWS) cone peak sensitivity (553 nm), and the 660-nm cut
on filter, at a significantly longer wavelength, were chosen to determine how
the sensitivity of the goby changed at wavelengths longer than the cone peak
sensitivities.
To ensure that the observed differences in RD were due to wavelength sensitivity and not brightness, all the RD studies were performed at two controlled irradiance levels (0.5 and 0.015 µmol m-2 s-1). The irradiance level in the experimental arena was controlled by adjusting the energy/W of the lamp and/or by adding layers of plankton cloth (a loosely woven white cloth made of polypropylene) between the light source and the interference filter. A spectroradiometer (LI-COR, LI-1800UW; Lincoln, New England, USA) was used to establish that no change in wavelength composition was caused by these dimming methods. The irradiance was measured over the range of 380-760 nm, using a Biospherical Instruments QSP-170B with a QSR 240 sensor (Lincoln, New England, USA).
G. flavescens uses a saltatory search (SS) or `pause-travel'
search (Utne, 1997). The SS
strategy is a punctuated repositioning movement, in which the predator only
scans for prey during a brief stationary period (search pause)
(Browman and O'Brien, 1992). If
the goby locates prey during the search pause, the pause is followed by an
attack. If prey is not located, the goby moves a little and stops again for a
new scanning pause. The distance between the last search pause, where the
reaction occurred, and the location of the attacked prey is defined as the
reaction distance (RD) (Vinyard and
O'Brien, 1976; Gregory and
Northcote, 1993). The reaction is characterised by a rapid tail
beat (`fast-start') (Webb,
1978; see also Gordon,
1983), which gives the fish an acceleration towards the prey.
Reaction distance
Experimental design
The experimental apparatus consisted of a 200x30x30 cm glass
aquarium that was divided into three compartments; two conditioning
compartments (50x30x30 cm) at each end of the aquarium, and a
central experimental compartment (100x30x30 cm). Sliding doors
connected the compartments (for details, see
Utne, 1997). Water was turned
off during the observation period, and water depth was maintained at 5 cm. The
experimental compartment had a 2x2 cm grid on the bottom. A remotely
operated video camera placed over the aquarium was used to record
observations. Live prey were introduced to the experimental arena in two glass
cylinders (2 cm in diameter and 10 cm tall). By placing the prey in a glass
cylinder, senses other than vision were eliminated. The cylinders were placed
randomly in the experimental compartment to minimise the influence of spatial
memory (Benhamou, 1994;
Noda et al., 1994).
In order to differentiate between the sensitivity of gobies to changes in
overall light intensity and changes at specific wavelengths, RD studies were
performed at two irradiance levels of 0.5 and 0.015 µmol m-2
s-1 at the five different spectral locations given above. Both of
the chosen light intensities are below the white light saturation level of
G. flavescens (8 µmol m-2 s-1)
(Utne, 1997). Calanus
spp. (length 3.0-4.0 mm) was used as prey, with transparent individuals being
selected in order to reduce the influence of contrast variability due to
wavelength. For further details of the methods, see Utne
(Utne, 1997) and Utne-Palm
(Utne-Palm, 1999).
Conditioning and observation
Ten gobies at a time (from a total of 20) were introduced into the
experimental aquarium for acclimatisation. The gobies were trained daily (1-2
h), over a 2-week period, to enter the experimental compartment and search for
prey. During the training, copepods were introduced to the compartment, which
taught the gobies to search the arena for food. Before each trial, gobies were
starved for 24 h, since hunger is known to influence (increase) RD
(Confer et al., 1978).
At the beginning of the experiment, the 10 gobies were kept in one of the two conditioning compartments, from which two fish at the time were introduced to the experimental compartment by opening one of the slide-doors (when needed, a net was used to hold back the rest of the fish from rushing in). Two fish were used, since the fish appeared stressed when isolated. During 10 randomly chosen observation periods an empty glass cylinder was placed in the experimental arena. No attacks or reactions to these empty tubes were ever observed. The gobies were conditioned to the experimental light conditions for 1.5 to 2 h before observation. Light conditions were randomised, with only one wavelength condition being tested on a single day. Between 15 and 20 fish were tested at each wavelength condition. Using only the longest observed RD of each tested fish, this yielded between 15 and 20 RD observations for each tested wavelength condition.
Optomotor response
Experimental design
The optomotor response was measured in an apparatus similar to the one used
by Krauss and Neumeyer (Krauss and
Neumeyer, 2003), consisting of a stationary glass
cylinder/experimental arena (9.15 cm diameter, 15 cm high) in which the tested
fish could swim freely. This glass cylinder was concentrically surrounded by a
cylinder (diameter 14.4 cm) consisting of 1 mm wide stripes made of white
cardboard and equally wide slits. The striped cylinder was placed on a clear
Plexiglas disk that could be rotated by a motor (Multifix, Constant, Germany)
at a velocity ranging from four rotations per min to one rotation per 2 min,
in both directions. The light source (described earlier) illuminated the test
tank and the white stripes of the rotating cylinder from above. The behaviour
of the fish was monitored from below by a video camera (Panasonic WV bp550)
with infrared filter (Optolite 50% IR) connected to a monitor (Panasonic,
WV-5340). The experimental setup was surrounded by black cloth to eliminate
stray light and to provide high contrast between the slits and white cardboard
stripes. At the lowest illumination levels, infra red (Derwent, MF100, 950 nm;
Birmingham, UK) was added to enhance camera visibility.
Conditioning and observation
The experimental fish was placed in the test tank to acclimatise to the
cylinder and the wavelength, 15 min prior to starting the motor rotating the
pattern. The recording of the optomotor behaviour started 30 s later, to avoid
recording an initial startle reaction shown by many fish. During a threshold
determination at each particular wavelength, the irradiance level (measured in
the glass cylinder/experimental arena) was reduced in steps of <0.05
µmol m-2 s-1. At each illumination level the fish was
given ten trials in which the direction of the rotating stripes varied
randomly during the test sequence. An illumination level was considered above
threshold if the fish followed the stripes in eight of the ten trials. Twenty
fish were used to test the six wavelengths, with five different fish tested at
each wavelength. Only five fish were used to test more than one wavelength,
since most of the fish became inactive after being tested for a while. When
one fish was used for more than one wavelength, the wavelengths were tested in
random order.
The gobies did not follow the stripes by swimming at a constant pace, but
instead jumped along with the stripes (in small steps). Their inability to
follow a visual stimulus at a constant pace is probably the result of their
saltatory search (SS) behaviour in which they only scan for prey or other
visual stimuli during brief stationary periods (search pause). Furthermore,
some fish jumped along only for a short distance and then doubled back,
started to follow another stripe, and so on, repeating the cycle. This
behaviour is similar to the optomotor behaviour of the goldfish described
(Cronly-Dillon and Muntz,
1965). Initially this last behaviour caused some difficulty, but
it became apparent that the movements the goby makes when it starts to follow
a stripe are different (short jumps with the eyes close to the glass wall)
from those that it makes when it starts to double back (longer jumps and eyes
not in close contact with the glass wall). Sometimes the goby placed itself in
the centre of the test tank, and simply rotated around its own axis following
the stripes, or occasionally some fish were inactive, lying on the bottom of
the test tank and following the stripes with their eyes. Data from fish
showing these types of behaviour were not used.
Data analysis
G. flavescens uses a SS strategy, searching for prey only during
stationary pauses. Some of the measured RDs will therefore be underestimates
because the prey items might be relatively close to the predator when the
predator stops for a pause. Maximum RD has therefore been used to describe the
visual ability of this (Utne,
1997) and other SS foraging planktivorous fish
(O'Brien and Evans, 1991).
Furthermore, the two-spotted goby is known to decrease its activity and
feeding rate with decreasing light, and in the dark they are inactive,
`sleeping' on the kelp or rocks (Gordon,
1983; Costello,
1992). Thus, in the present study their feeding motivation should
be quite low, since very low illumination levels were used. At the lowest
irradiance level (0.015 µmol m-2 s-1) there were a
large number of very short RDs, independent of wavelength, which was not the
case in the higher irradiance treatment (0.5 µmol m-2
s-1). Therefore, to make sure that only the most motivated fish was
used in the analysis, we chose to use only the five longest RDs measured (from
five different fish) at each wavelength and illumination level.
Two-way analysis of variance (ANOVA) was used to resolve any significant relations between RD, wavelength and illumination conditions. An ANOVA, post hoc test (Neuman-Keuls) was used to test for differences in RD between wavelengths within each illumination level. In addition, an ANOVA, post hoc test (Neuman-Keuls) was used to test for differences in RD between illumination levels within each wavelength. RD raw data were log transformed to achieve a normal distribution.
The optomotor response results were also treated with an ANOVA, post hoc test, to test for differences in illumination threshold between the different wavelengths.
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max of the rods was at about 508 nm and there was a
population of small short-wave-sensitive (SWS) single cones with
max close to 456 nm. The majority of double cones were
identical middle-wave-sensitive (MWS) cones with both members containing a
531-nm pigment, though a small number of identical long-wave-sensitive (LWS)
double cones with max at about 553 nm and non-identical
double cones, with the 553-nm and 531-nm pigments, were also identified. In
addition, there were small populations of large single cones, the majority of
which contained the MWS 531-nm pigment, but with a small number of cones
containing the LWS 553-nm pigment. We cannot exclude the possibility that
these represent double cones in which the two members have become separated.
For details of the max, transverse absorbance and the
number of cells analysed, see Table
1 and Fig. 1. There
was no difference between the sexes in numbers and types of visual
pigments.
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Lens transmission
The lens (Fig. 1F) shows
maximum transmission from 700 nm through into the shorter wavelengths, with a
clear cut-off at about 410 nm. Transmission was therefore greatly reduced in
the ultraviolet below 410 nm.
Reaction distance
A two-way ANOVA revealed that both wavelength
(F5,160=62.8, P<0.00001) and illumination
(F1,160=219.2, P<0.00001) had a significant
effect on RD, and that there was an interaction between wavelength and
illumination (F5,160=6.6, P=0.00001). Owing to
the interaction between wavelength and illumination level, an ANOVA post
hoc test (Newman-Keuls) was conducted for each illumination level. This
test revealed that RD at 0.5 µmol m-2 s-1 was longest
at 532 nm (MWS matching light), but not significantly longer than at 550 nm
(LWS matching light). The RD was significantly longer at 510 nm (rod matching
light) than at 460 nm (SWS matching light) and >660 nm, but was
significantly shorter than at 532 and 550 nm (ANOVA, P<0.01). For
the same wavelengths, but at the lower irradiance of 0.015 µmol
m-2 s-1, there was no difference in RD found between the
max matching wavelengths (460, 510, 530 and 550 nm) (ANOVA,
P>0.01), with the exception of a shorter RD at 460 nm compared to
530 nm (P=0.026). In addition, RD was significantly shorter at the
longer, non-pigment matching wavelengths (>660 nm and 560 nm), compared to
the pigment matching wavelengths (ANOVA, P<0.05).
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Optomotor response
Wavelength composition had a significant effect on the sensitivity of the
goby (one-way ANOVA, F5,4=143,P<0.0001). The
ANOVA post hoc test (Newman-Keuls) revealed that there was a
significant difference in sensitivity at all wavelengths, with the exception
of 510 nm (rod matching light) and 560 nm, and between 530 nm (MWS matching
light) and 550 nm (LWS matching light)
(Fig. 2B).
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;
Loew and Lythgoe, 1978;
Lythgoe, 1979).
The visual pigments reported here for G. falvescens fit
comfortably into this pattern with the retina dominated by MWS double cones.
However, the pigments in the double cones are somewhat different from those
published previously for the two-spotted goby
(Partridge, 1990). The data
for the rods and SWS small cones are similar, but the MWS and LWS pigments are
noticeably different; 525 and 570 nm
(Partridge, 1990), but 531 and
553 nm in the present study. This discrepancy is difficult to explain, but
could suggest differences between individuals from the southwest of England
(Partridge, 1990) and those
from Norway. Nevertheless, this combination of cones, which form a square
mosaic of four double cones, maximally sensitive at longer wavelengths,
surrounding a central small single SWS cone is typical of shallow coastal
water species (Loew and Lythgoe,
1978; Lythgoe,
1979). The lack of UV-sensitive cones is also a common feature of
inshore fish and, in the goby, correlates with the lens transmission that
effectively cuts off light below about 410 nm
(Losey et al., 2003;
Thorpe et al., 1993).
The aim of the present investigation was to explore the spectral
sensitivity of the two-spotted goby, from a physiological and behavioural
perspective, and to test the hypothesis that the goby would be more sensitive
to a change in illumination level at its pigment maxima than away from the
pigment maxima. G. flavescens is a shallow water (0-10 m depth)
species, which, therefore, experiences a great range of illumination levels
(1000-20 µmol m-2 s-1 at the surface on a sunny day
or on a cloudy winter day, respectively) as well as wavelength. An
illumination level similar to the one chosen in the present study is
representative of the top 3-10 m of the water column during a spring or autumn
algal bloom (Utne-Palm,
2004).
The RD data at the higher irradiance of 0.5 µmol m-2
s-1 (
26 lux) shows a spectral sensitivity function with a
maximum around 530-550 nm. The maximum RD observed at 550 nm in the present
study was 35 cm, which is much greater than the 22 cm measured in an earlier
study using white light of 8 µmol m-2 s-1 (400
lux) from a halogen light source (Utne,
1997). [In the same study
(Utne, 1997) 8 µmol
m-2 s-1 was found to be the light saturation level for
the two-spotted goby, and 20 µmol m-2 s-1 was found
to be the level of increasing dazzle effect.] The fact that lower illumination
was needed to obtain a long RD when light was composed of wavelengths close to
the maximum sensitivity of the majority of cones, than when light was composed
of wavelengths away from this peak, clearly demonstrates the
importance of the spectral composition of the available light. Increasing the
irradiance level from 0.015 µmol m-2 s-1 (0.8
lux) to 0.5 µmol m-2 s-1 (26 lux) led to a
significant increase in RD for all wavelengths, with the exception of 460 nm
(SWS matching light) (Fig. 2A).
The positive effect of an increase in illumination was most pronounced at 530
nm (MWS matching light) and 550 nm (LWS matching light)
(Fig. 2A). Thus, at the higher
illumination, there is a clear correlation between the spectral sensitivity of
the RD and the peak sensitivity of the double cones. This is the most
straightforward comparison, since the majority of the double cones are
identical doubles with a 531-nm pigment, but a small contribution from the LWS
pigment of some double cones to a luminosity sensitivity function cannot be
excluded. However, at the lower illumination, which is clearly scotopic to the
human eye, such a correlation is not so clear. At this low light level, the RD
is greatly reduced, though still maintaining a peak around 530-550 nm. The
relatively smaller reduction in RD at shorter wavelengths may represent either
a greater input from SWS cones, or more probably, evidence of a rod intrusion
at these low light levels (Fig.
2A).
The optomotor results identify a somewhat similar spectral sensitivity to
the RD responses at the higher light intensity
(Fig. 2B). However, the peak is
at slightly longer wavelengths at 550 nm, which could indicate that the
optomotor response is driven not only by the dominant MWS identical double
cones, but also by input from the LWS cones of the minority population of
non-identical double cones. This would be in agreement with findings in
goldfish (Schaerer and Neumeyer,
1996) and zebrafish (Krauss
and Neumeyer, 2003) where motion detection appears to be driven
primarily by LWS cones. However, the narrow sensitivity function obtained in
the present study suggests that the optomotor response may be driven by a more
complex chromatically opponent input. This is supported by monochromatic
rearing studies in the cichlid, Aequidens pulcher
(Kröger et al., 2003),
which showed significant changes in optomotor responses to chromatic
stimuli.
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