Rearing in different photic and spectral environments changes the optomotor response to chromatic stimuli in the cichlid fish Aequidens pulcher
1 Eberhard-Karls University Tübingen, Institute of Anatomy,
Österbergstrasse 3, 72074 Tübingen, Germany
2 Lund University, Department of Cell and Organism Biology, Vision Group,
Zoology Building, Helgonavägen 3, 22362 Lund, Sweden
* Author for correspondence (e-mail: ronald.kroger{at}cob.lu.se)
Accepted 26 February 2003
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Summary |
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Key words: color vision, spectral processing, developmental plasticity, vertebrate, cichlid fish, Aequidens pulcher
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Introduction |
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In contrast to findings concerning early stages of chromatic processing,
previous studies on higher neural levels (from optic nerve fibers to behavior)
reported no or small effects of spectral and/or visual deprivation in a
variety of vertebrate species (primates,
Boothe et al., 1975; Brenner et
al., 1985
,
1990
;
Di et al., 1987
; ground
squirrels, McCourt and Jacobs,
1983
; tree shrews, Petry and
Kelly, 1991
; ducks, Peterson,
1961
; pigeons, Brenner et al.,
1983
; and goldfish, Mecke,
1983
). These findings had suggested that the developmental program
of spectral processing and color vision is genetically determined. We now
report that rearing A. pulcher in different visual environments not
only induces neural plasticity in the retina but also changes behavioral
responses to chromatic stimuli.
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Materials and methods |
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Optomotor response
In the optomotor response, animals follow a moving visual pattern if there
are no other stronger cues for orientation. To elicit the behavior, we
presented pairs of patterns moving in opposite directions, similar to the
apparent motion stimuli used by Neuhauss et al.
(1999).
The dimensions of the experimental tank were 2.0 m0.25 m
0.25 m
(length
width
height). The front wall was covered with white
adhesive film on which the stimulation patterns were projected. The other
walls were black, and the bottom was of dark-red color that absorbed almost
all visible light but diffusely reflected far-red and near-infrared
wavelengths. We used a data projector (Mitsubishi L VP-X-100E) to project
moving (0.17 m s1) pairs of sinusoidal vertical gratings (38
cycles m1) on the front wall of the experimental tank. The
two gratings had opposing gradients of brightness and directions of motion,
with each grating moving towards its darker portion
(Fig. 1A). The spectra and the
gradients of brightness of the projected lights are shown in
Fig. 1B,C. The animals followed
the grating they perceived as brighter down its intensity gradient until they
reached the point of equi-luminance between the two gratings. At this
location, the animals experienced a balanced, converging motion stimulus from
both sides. This is similar to the visual flow field during backward motion.
In response, the animals swam forward against the wall of the tank. They
remained at the front wall of the experimental tank within a narrow lateral
region including the point of equi-luminance, thereby indicating which
relative strengths the presented gratings had to drive the optomotor
response.
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The experimental schedule is illustrated in Fig. 1D. Each fish was exposed to light of spectral composition different from the rearing light for only about 30 min, including the time the fish was given to familiarize itself with the experimental tank.
For recordings, the experimental tank was illuminated from above with infra-red light-emitting diodes (peak emission at 875 nm). The animals were video-taped with an infra-red-sensitive CCD camera (BC-2, AVT Horn). After each change in the direction of grating motion or combination of colors, we waited for 20 s to allow the fish to find the new point of equi-luminance. Then, five images were grabbed at intervals of 10 s. For analysis, the tank was divided into 19 bins of 10 cm in width (15 cm for bins 9 and +9, which were rarely visited by the animals). Bin number 0 was at the centre of the tank. The binned positions of the fish were digitally determined from the grabbed images (25 measurements), switched between left and right in parallel to the switches in color positions, and averaged for each combination of colors before further analysis.
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Results |
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Statistically significant (by analysis of variance) effects of the rearing conditions were detectable by stimulation with blue/red and green/red color pairs (Table 1). Rearing blue acara in long-wavelength light (red group) did not change the points of equi-luminance. Rearing in middle-wavelength (green group) and short-wavelength (blue group) light resulted in a significant shift of the point of equi-luminance towards long wavelengths (Table 2; Fig. 2). This indicates that the animals were less sensitive to long-wavelength light than the animals in the DW reference group (or more sensitive to middle- and short-wavelength light, or a combination of both effects). In the BW group, short and middle wavelengths were more efficient relative to long wavelengths in driving the optomotor response than in the DW group (Table 2; Fig. 2).
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Sources of variance
`Failures' of fish to react to a change of color positions occurred in
approximately 10% of all runs. When the fish was in bin N during one
orientation of colors, the same position was assigned to bin N after
the change in color positions. Even small numbers of failures therefore led to
large amounts of variance among measurements and fishes
(Table 1). Furthermore, group
means were somewhat biased towards 0 (centre of aquarium). We did not
eliminate any `bad' runs from the analysis because it was impossible to detect
them by criteria that were objective and equally applicable to all data sets.
When the fish remained stationary close to the centre of the aquarium, it was
unclear whether the animal had ceased to react or whether it was at its point
of equi-luminance. Furthermore, when a fish remained at the same position in
the aquarium during a cycle of changes in color positions, we could not
determine whether N or N was the real point of equi-luminance.
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Discussion |
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In agreement with the observations in the outer retina, rearing in red
light had no effect on the optomotor response
(Fig. 2;
Table 2). In the other rearing
groups, however, the results differed somewhat from what was expected from the
findings in the outer retina. When long wavelengths were tested against middle
and short wavelengths, the fish in the green and blue groups had virtually
identical points of equi-luminance, which differed significantly from the DW
group. In studies on the outer retina, the green group had been similar to the
DW group (synaptic complexes of cones,
Kröger and Wagner, 1996;
survival of short-wavelength-sensitive cones,
Kröger et al., 1999
;
Wagner and Kröger, 2000
).
With the reservation that fewer fish could be tested in the green group
(N=7) than in the other groups (N=12), our current findings
suggest that the mechanisms controlling spectral sensitivity in the blue acara
are more complex than a simple short vs long wavelength compensation.
Furthermore, it is likely that regulatory mechanisms are present on several
levels of chromatic processing, since the effects observed in the outer retina
cannot fully explain the effects on the behavioral level.
The existence of several levels of compensatory mechanisms is also
suggested by a preliminary observation of an effect of rearing in red light.
In fish reared in red light, a substantial proportion of
short-wavelength-sensitive (SWS) cones was eliminated after the animals had
been transferred to white light. We suggest that this might serve to
counter-compensate in the outer retina for a compensation on a higher level
induced by the initial rearing under red light
(Wagner and Kröger,
2000).
Comparison with other species
In light of the strong effects of spectral deprivation on retinal
morphology and visual behavior in the blue acara, it seems surprising that
similar effects have not been found in other vertebrates. A likely reason is
that most research groups used long-wavelength light during rearing
(Peterson, 1961;
McCourt and Jacobs, 1983
;
Brenner et al., 1985
,
1990
), which turned out to be
ineffective in the blue acara too. Closest to our study is the work on
goldfish (Carassius auratus) by Mecke
(1983
). In that and our
studies, fish were reared for long times (>1 year) under narrow-banded
lights of short and long wavelengths. In contrast to our approach, Mecke
initially used a training paradigm that exposed the monochromatically reared
fish to various spectral lights for about a week prior to testing. When these
experiments did not reveal any significant differences in color discrimination
ability between control and monochromatically reared animals, the author
surmised that the goldfish might have recovered from the effects of spectral
deprivation during the training period. Some animals reared in red light were
therefore trained only under red light before testing. Even under those
carefully controlled conditions, no significant effect of spectral deprivation
was detected (Mecke, 1983
).
This is in agreement with our results, since changes in the optomotor response
of the blue acara were only present in the blue and green groups and not in
the red group.
Pigeons reared in red and blue lights were also tested only after they had
been exposed to broad-spectrum light for some time
(Brenner et al., 1983). The
apparent differences between our findings and the results of earlier studies
may be resolved when more is known about the time-scale of recovery from the
effects of spectral deprivation.
Interestingly, developmental plasticity in color vision has recently been
demonstrated in a mantis shrimp (Haptosquilla trispinosa, Stomapoda);
Cronin et al., 2001].
Developmental fine-tuning of spectral sensitivity and processing may be
present in many visual systems.
Effects of the intensity of white light
It may seem surprising that the intensity of white light during rearing
induced changes in the optomotor response to stimuli of different colors
(Table 2;
Fig. 2). The functional
explanation for this phenomenon might be found in photoreceptor noise. Rieke
and Baylor (2000) have shown
that the dark noise of long-wavelength-sensitive (LWS) cones of the salamander
is dominated by thermally induced isomerisations of the photopigment, while
the dark noise of SWS cones has other origins. Even in complete darkness,
thermally induced isomerisations keep the LWS cones in a partially
light-adapted state, such that their responses to dim flashes are much lower
than those of SWS cones (Rieke and Baylor,
2000
). Such pre-adaptation of LWS cones by dark noise only plays a
role in dim light, since in bright light all cones will be in the
light-adapted state. In our DW group, pre-adaptation of the LWS cones may have
reduced their signals relative to SWS cone signals. In response, compensatory
mechanisms during rearing may have increased the gain in channels processing
LWS cone signals and/or reduced the gain in channels processing SWS signals,
making the animals from the DW group during testing relatively more sensitive
to long-wavelength light than fish from the BW group
(Table 2;
Fig. 2).
Previously, we have observed effects of the intensity of white light at the
level of cone-specific horizontal cells (CHCs). Rearing in bright white light
led to a significant reduction of synaptic contacts between SWS cones and CHCs
of the H2-Cb type, which biphasically encode chromaticity
(Braun et al., 1997).
Furthermore, the spectral responses of H2-Cb cells differed significantly
between the DW and BW groups (Kröger
et al., 2001
). In fishes, the strength of feedforward signalling
by cones is influenced by sign-inverting feedback from CHCs to the cones'
output synapses (Stell et al.,
1994
; Kamermans and
Spekreijse, 1995
; Kamermans et
al., 2001
). Such feedback from CHCs to cones may have a role in
bringing about the effects of light intensity.
Input channels to the optomotor response
Under mesopic conditions, input from both cones and rods may contribute to
the optomotor response. Since the gratings were projected over a large area
and were viewed from behind the white film that served as a projection screen,
light intensities during chromatic stimulations
(Fig. 1C) may have been in the
mesopic range. It is nevertheless unlikely that rods made any contribution to
the optomotor responses investigated in this study. In the blue acara, the
retinomotor movements of cones, rods and melanosomes in the retinal pigment
epithelium cells (Burnside and Nagle,
1983) are strongly influenced by a circadian oscillator. In the
light-adapted state, only cones are in the focal plane of the eye. The myoids
of rods are elongated and their outer segments are screened from incoming
light by the melanosomes of the retinal pigment epithelium. Once entrained to
a daily light:dark cycle, rods and cones remain in their light-adapted
positions throughout the entire light phase, even during prolonged darkness
(Douglas et al., 1992
). During
morphological studies (Kröger and
Wagner, 1996
; Braun et al.,
1997
; Kröger et al.,
1999
), we observed that cones contracted fully in animals reared
in long-wavelength light. A slight reduction of the contraction of single
cones present in young animals (6 months old;
Kröger and Wagner, 1995
)
was not found in adults (R. H. H. Kröger, B. Knoblauch and H.-J. Wagner,
unpublished observations).
Schaerer and Neumeyer
(1996) have reported that the
optomotor response of the goldfish receives positive input only from LWS cones
and that there seems to be only weak negative input from SWS cones. By
contrast, the optomotor response of A. pulcher seems to be driven by
several spectral cone types. Involvement of rods is unlikely (see above) and
the absorbances of the cone pigments were insensitive to the rearing
conditions (Kröger et al.,
1999
). If a single spectral cone type drives the response, all
animals should have had identical relative sensitivities to the pairs of
colors used in this study. Our results therefore suggest that several spectral
types of cone are involved and that their relative contributions, which may be
positive and negative, to the optomotor response are influenced by the
spectral environment during development.
This should be kept in mind during comparisons of visual capabilities of different stocks of animals. Different results from different groups of conspecifics may not only be due to genetic differences and different procedures if several research groups are involved but may also be caused by different lighting conditions during development of the animals.
Dorsal light reaction
If illuminated from the side, fish orient their dorso-ventral body axis
parallel to a vector resulting from the addition of the gravity vector
(vertical) and the light vector (horizontal)
(von Holst, 1935). The
brighter the light, the more strongly the animals tilt towards the light
source. This dorsal light reaction has previously been used to determine
spectral sensitivities in other fish species
(Silver, 1974
;
Powers, 1978
). A.
pulcher, however, showed only negligible tilt when illuminated with light
levels that induced an almost 90° tilt in the goldfish we used for
comparison. The dorsal light reaction in A. pulcher was thus too weak
to be used for measurements of spectral sensitivities.
Conclusions
The optomotor response of A. pulcher to chromatic stimuli is
dependent on the spectral and photic conditions during rearing. This and
previous findings indicate that in this species developmental plasticity is
not only present in the retina but is also evident at the behavioral level.
The circuitry of spectral processing and color vision in vertebrates may
therefore not be as strictly genetically determined as has been suggested by
the results of earlier studies.
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Acknowledgments |
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