Circadian rhythms of behavioral cone sensitivity and long wavelength opsin mRNA expression: a correlation study in zebrafish
1 Department of Physiology, University of Kentucky College of Medicine,
Lexington, KY 40536 USA
2 Department of Biology, University of Victoria, British Columbia, V8W3N5
Canada
3 Department of Biological Sciences, University of Notre Dame, Notre Dame,
IN 46556 USA
* Author for correspondence (e-mail: li.78{at}nd.edu)
Accepted 1 December 2004
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Summary |
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Key words: circadian rhythm, opsin mRNA expression, behavioral visual sensitivity, zebrafish
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Introduction |
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Ample evidence suggests that in addition to the endogenous circadian
control, external cues, such as light and dopamine, play important roles in
circadian visual function. Light produces acute effects; shorter periods of
light exposures may shift the circadian rhythms (Cahill and Besharse,
1991,
1993
), whereas prolonged
periods of light exposures may diminish them
(Green and Besharse, 1996
;
Li and Dowling, 1998
).
Dopamine plays a modulatory role in circadian rhythms of photoreceptor
sensitivity (Ko et al., 2003
)
or behavioral visual sensitivity (Li and
Dowling, 2000
). The underlying mechanisms of light and dopamine on
circadian visual sensitivity may vary, e.g. by activating different second
messenger pathways (Ribelayga and Mangel,
2003
), or by phase-shifting the expression of immediate-early
circadian genes (Steenhard and Besharse,
2000
).
While circadian oscillation in behavioral visual sensitivity and opsin expression has been well documented, the questions remain whether the behavioral visual sensitivity is correlated with opsin gene expression, and if a correlation exists, whether the cyclic expression of opsin is the sole factor limiting the circadian rhythm in behavioral visual sensitivity. We demonstrate that in zebrafish the circadian rhythm of behavioral cone (red cone) sensitivity was correlated with LC opsin mRNA expression, but only for about 24 h. Thecircadian cycle in LC opsin mRNA expression was also shown to be regulated by light and dopamine.
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Materials and methods |
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Behavioral analysis of zebrafish cone sensitivity
Methods for behavioral analysis of zebrafish visual sensitivity have been
previously described (Li and Dowling,
1997; for a review, see Li,
2001
). The test apparatus consisted of a circular plastic
container, surrounded by a rotating drum. A black segment was marked on white
paper that was attached to the inside of the drum. The drum was illuminated
from above by a halogen lamp, filtered with a 620 nm band-pass interference
filter (10 nm half max bandwidth; Oriel Instruments, CT, USA). The maximum
light intensity at the water surface in the container was log 0=40 µW
cm-2. The light intensity was adjusted by changing neutral density
filters at 0.5 log unit steps.
Zebrafish display robust escape responses to the black segment rotating
outside the container, for example, they rapidly reverse their swimming
direction when encountering the black segment
(Li and Dowling, 1997). In
this study, we measured red cone sensitivity by recording the lowest intensity
of red light required to evoke escape responses. Red light (>600 nm)
activates primarily the red cone photoreceptor cells
(Robinson et al., 1993
;
Brockerhoff et al., 1997
).
Thus, the escape response evoked under the near-threshold red illumination is
unlikely mediated by other types of photoreceptor cells such as rods, which
have a
max at about 500 nm
(Nawrocki et al., 1985
;
Cameron, 2002
;
Chinen et al., 2003
). Prior to
visual threshold measurements, the fish were dark adapted for 15 min. This
timing is sufficient to dark adapt the cone system in zebrafish
(Li and Dowling, 1997
;
Ren and Li, 2004
). Normally,
we observed the fish behaviors for 1015 s, during which time the fish
encountered the rotating segment 24 times. A minimum of two escape
responses was required to score a threshold. The light illuminating the test
apparatus was initially set at a dim level, log I=3.0. If no escape
response was observed, the light was increased by 0.5 log unit steps until an
escape response was elicited. Infrared night vision goggles were used to
handle the fish at night or when the experiments were performed in DD.
Drug administration
Drug treatments were performed using isolated eyecups. Eyecups (two eyecups
for each sample collection) were prepared in the late afternoon the day before
the experiments were performed. Zebrafish were anesthetized with 1%
3-aminobenzoic, then they were decapitated. Eyes were enucleated and cornea
and vitreous body were removed. Eyecups were incubated in L15 media (Sigma,
MO) overnight in the dark. Prior to drug treatment, dopamine or dopamine
D1 (SKF38393 or D2 (quinpirole) receptor agonists
(Sigma, MO) were dissolved in phosphate buffered saline, pH 7.0, and diluted
in distilled H2O to 100 µmol l-1
(Lin and Yazulla, 1994). Drugs
were added to L15 culture media via micropipettes. The final
concentrations of dopamine in the culture media were 0.1 µmol
l-1, 0.5 µmol l-1, 1 µmol l-1 and 10
µmol l-1, respectively, and for D1 or D2
agonist, 0.1 µmol l-1, 1 µmol l-1, and 10 µmol
l-1, respectively. After 30 min of drug treatment, the eyecups were
removed from the media, and were transferred to RNA wiz (Ambion, TX, USA).
Samples were stored at 80°C. All drug treatments were performed in
the dark. Infrared night vision goggles were used to handle the samples in the
dark.
Total RNA extraction and real-time RTPCR
Total RNA was extracted from the eyes or cultured eyecups (in the case of
drug treatment). Eyes or eyecups (two for each sample collection) were
homogenized in 500 µl of RNA wiz (Ambion, TX, USA), followed by chloroform
extraction. RNA was precipitated with isopropanol, washed with 75% ethanol,
and re-suspended in 20 µl distilled H2O (RNAse free). The
concentration of total RNA was determined using a BioMate 3 series
spectrophotometer (Thermo Spectromic, NY). Red cone opsin specific primers and
probes (GenBank sequence accession number, AF109371; 5'-TGG AGC AGA TAC
TGG CCT CAT-3' and 5'-GGG TCC TCG CTT CCA CTG A-3'; TaqMan
probe, 5'-TCT GAA GAC CTC CTG TGG CCC TGA TG-3') were designed
using the Primer Express Primers system (ABI, CA, USA).
Real time RTPCR was performed using the TaqMan One-Step RTPCR Master Mix Reagents Kit (ABI, CA, USA). The reaction (25 µl) contained 2 ng total RNA, 300 nmol l-1 primers, and 250 nmol l-1 probe. Reactants were mixed and transferred into a 96-well PCR plate, with 2 µl (1 ng ul-1) of total RNA in each well. Each sample was run in duplicate along with control reactions, which did not include the addition of reverse transcriptase or template. TaqMan ribosomal RNA was used as an internal control. The thermo cycling conditions were 30 min at 48°C, 10 min at 95°C, 45 cycles of 15 s at 95°C, and 1 min at 60°C. Relative LC opsin mRNA expression was determined using the standard curve method provided by ABI. Standard dilution curves of cDNA were generated for both LC mRNA and rRNA control. The cDNA was synthesized using Superscript First-Strand Synthesis System (Invitrogen, CA, USA) using 5 µg of total RNA from each sample in 40 µl total volume. The reaction was performed by the same method described above except that there was no reverse transcriptase added. The dilution values of 1, 0.25, 0.0625, 0.0156, 0.0039, 0.0010 and 0.00025 were used to generate the standard curve. To normalize the data to the endogenous control rRNA, the amount of LC opsin mRNA and rRNA were determined from the standard curve for each sample. The amount of LC opsin mRNA was divided by the amount of rRNA. Relative LC opsin mRNA expressions (during a 24 h period in LD or LL or DD) were determined by dividing the concentration of LC opsin mRNA obtained at each time in the day and night by the concentration of LC opsin mRNA obtained at 07:00 h.
Microspectrophotometry (MSP)
MSP was performed to determine the absorbance maximum
(Amax) of the red cones. The microspectrophotometer used
in this study has been previously described
(Hawryshyn et al., 2001). In
brief, short duration flashes (0.05 s) of full spectrum (300800 nm)
unpolarized (beam size, 2x3 µm) light from a 150 W xenon light source
were delivered to the photoreceptor outer segments. The transmitted beam
passed through a spectrometer (300 nm blazed grating; Acton Res Co, MA, USA)
and onto a 1340x400 pixel Peltier cooled (55°C)
back-illuminated CCD detector (Princeton Instruments, NJ, USA). Photoreceptor
absorbance [log10 (1/T)] was calculated by comparing the
transmitted intensity through the photoreceptor (Im) to
the transmitted intensity through an area clear of debris adjacent to the
photoreceptor [reference (Ir) thus,
T=Im/Ir].
Amax was recorded in mOD, which is a measure of optical
density (1 mOD=10-3 OD).
Zebrafish were dark adapted for 1 h prior to dissection under infrared
illumination. Once on the CCD-MSP microscope, samples were examined under
infrared illumination and monitored by an infrared camera. The infrared image
was transmitted to a computer that also served as the central control unit for
the CCD-MSP device. While searching the retinal sample for long-wavelength
sensitive cones the path of the motorized stage was plotted on screen to
eliminate the possibility of recording from the same photoreceptor more than
once, which would result in an underestimate of the Amax.
Once recorded the absorbance spectra were stored for later analysis. Using an
analysis program the Amax was automatically calculated
from the peak of the max to the baseline. The main estimate
of
max was determined by a minimum variance fit to the
upper 20% of the absorption spectrum
(Govardovskii et al., 2000
).
An independent sample t-test was used to compare the mean
Amax values determined in the day and night.
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Results |
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The fluctuation in behavioral cone sensitivity persisted in the zebrafish
that were kept in constant conditions. In DD, cone sensitivity was low in the
subjective early morning and high in the subjective late afternoon, similar to
the fluctuation of cone sensitivity determined in LD. The threshold difference
between the subjective early morning and late afternoon, however, was slightly
reduced in DD as compared to the threshold difference determined in LD. In the
first day of DD, for example, between subjective 07:00 and 19:00 h
thedifference in behavioral cone sensitivity was 0.8±0.2 log units. On
the second day of DD, it was further reduced, to 0.6±0.2 log units
(Fig. 1). It has been
previously shown that the fluctuation of behavioral visual sensitivity
persisted in DD for 57 days before it completely dampened out (see
Li and Dowling, 1998).
LC opsin mRNA expression fluctuated in correlation with behavioral cone sensitivity
We measured LC opsin mRNA expression at different times in the day and
night using real time RTPCR. In LD
(Fig. 2A), the expression of LC
opsin mRNA was low in the early morning and high in the late afternoon. The
lowest expression was observed at 07:00 h. The expression increased through
the mid-morning and early afternoon, and reached the highest level in the late
afternoon at 19:00 h. From 07:0019:00 h, theexpression of LC opsin mRNA
increased approximately 50-fold. Shortly after light offset, the expression of
LC opsin mRNA began to decrease. By 22:00 h, the expression had decreased to
levels about one half of the peak level determined at 19:00 h. By 04:00 h in
the second day, the expression of LC opsin mRNA decreased to levels about one
half of the level seen at 22:00 h.
|
Under constant darkness, the circadian oscillations in the expression of LC opsin mRNA persisted for approximately 24 h. In the first day of DD (Fig. 2A), the expression of LC opsin mRNA was low in the subjective early morning and high in the subjective late afternoon and early evening, similar to the fluctuation of LC opsin mRNA expression in LD. During the subjective day, the expression of LC opsin mRNA increased. Between subjective 07:00 and 19:00 h, the expression of LC opsin mRNA increased about 40-fold. During the subjective night, however, the expression of LC opsin mRNA decreased only slightly. At subjective 04:00 h, the expression was significantly higher than the expression determined at 04:00 h in LD. In the second day of DD, no obvious fluctuations of LC opsin mRNA expression were seen, i.e. at all times during the subjective day and night, the expression was similar to that determined at the end of the first day of DD.
We also measured LC opsin mRNA expressions in LL. In the first 24 h of LL, the expression of LC opsin mRNA was low in the subjective early morning and high in the subjective late afternoon and early evening (Fig. 2B). Between subjective 07:00 and 19:00 h, the expression of LC opsin mRNA increased about 40-fold. At subjective night, the expression decreased, in a similar fashion as seen in LD. By 04:00 h, the expression of LC opsin mRNA decreased to levels similar to those determined in the early morning in control animals. In the second day of LL, no obvious fluctuations of LC opsin mRNA expression were seen, i.e. at all times between the subjective day and night, the expression was similar to that measured at 07:00 h in LD or at subjective 07:00 h in the first day of LL.
LC opsin density was high in the day and low at night
We measured opsin expression using MSP to determine if the fluctuation of
behavioral cone sensitivity and LC opsin mRNA expression was correlated with
long-wavelength-sensitive cone opsin expression. Optical density of the
long-wavelength sensitive cone was measured using MSP at 07:00, 12:00 and
22:00 h, respectively. The mean max was 558 nm. Our
estimate of
max is a close match to previous values
reported for adult zebrafish (Nawrocki et
al., 1985
; Cameron,
2002
; Chinen et al.,
2003
). All absorbance spectra conformed to the Govardovski et al.
(2000) template for vitamin A1-based visual pigments. The mean
Amax at 07:00 and 12:00 noon was 18.38±0.99 mOD
(N=44) and 22.17±0.76 mOD (N=75), respectively, and
at 22:00 h, 18.34±0.70 mOD (N=59)
(Fig. 3). An independent sample
t-test showed that at 12 noon the long-wavelength sensitive cone
opsin density (Amax) was significantly
(P<0.001) increased relative to measurements made at 07:00 and
22:00 h.
|
Dopamine increased LC opsin mRNA expression in the early morning
We examined whether dopamine has an effect on the circadian rhythms of LC
opsin mRNA expression. The experiments were performed at two different times,
one in the early morning, when LC opsin mRNA expression is low, and the other
in the evening, when LC opsin mRNA expression is high. Dopamine increased LC
opsin mRNA expression in a dose-dependent manner, but only in the early
morning (Fig. 4A). In the
morning, when treated with 0.1 µmol l-1 dopamine, the expression
of LC opsin mRNA increased to levels about 1.6±0.2-fold higher than the
expression seen in control samples (P<0.01). When the dopamine
concentration was increased to 10 µmol l-1, the expression of LC
opsin mRNA increased further to levels 2.0±0.5 fold of the control
expression (P<0.01). No obvious changes occurred in LC opsin mRNA
expression following dopamine administration when the experiments were
repeated in the evening (P>0.01)
(Fig. 4B).
|
The effect of dopamine on LC opsin mRNA expression is likely mediated by dopamine D1 receptors. In the morning, LC opsin mRNA expression increased when the eyecups were incubated for 30 min with dopamine D1 receptor agonist, SKF38393(Fig. 5A). The increase of LC opsin mRNA expression by SKF38393is dose-dependent. When treated with 0.1 µmol l-1 SKF38393 LC opsin mRNA expression increased to levels about 1.3±0.2 fold higher than the control expression (P=0.08); when treated at 1.0 µmol l-1, 1.8±0.7-fold (P<0.01); at 10 µmol l-1, 2.3±0.8-fold (P<0.01).
|
Activation of dopamine D2 receptors (by quinpirole) produced
little effect on LC opsin mRNA expression
(Fig. 5B). Although there was a
tendency of increased LC opsin mRNA expression, in most cases the increase was
not statistically significant (P>0.01). This increase may be due
to a cross reaction between quinpirole and dopamine D1 receptors.
It has been shown that D2 receptors are 23 orders of
magnitude more sensitive to dopamine than D1 receptors, and that
D2 receptors are expected to be activated at much lower
concentrations, i.e. nanomolar (Witkovsky
and Dearry, 1992; Missale et
al., 1998
).
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Discussion |
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Photoreceptor cells found in the pineal organ in the dorsal diencephalon
(Kelly and Smith, 1964;
Wilson and Easter, 1991
;
Forsell et al., 2001
; Gothilf
et al., 1999
,
2002
) may also play a role in
circadian vision. The zebrafish pineal organ functions rhythmically in the
absence of external time cues. For example, when cultured, the pineal organ
continues to release melatonin in a circadian manner under constant lighting
conditions (Cahill, 1996
).
Cone-like photoreceptor cells have been identified in the pineal
(Hendrickson and Kelly, 1971
;
Pu and Dowling, 1981
;
Allward et al., 2001
). These
pineal cones express opsins as well as other genes that may or may not be
expressed in retinal photoreceptor cells. In zebrafish nrc mutants,
for example, the photoreceptor cells in the retina are degenerated, however,
pineal photoreceptor cells are spared. In nie mutants, by contrast,
degenerations are seen in both the retina and the pineal photoreceptor cells
(Allward and Dowling, 2001
).
Circadian gene expression in the pineal photoreceptor cells may provide cues
to the retina through centrifugal pathways. Centrifugal modulation of visual
sensitivity has been previously reported in Limulus
(Barlow et al., 1980
;
Battelle, 1991
) and in
zebrafish (Maaswinkel and Li,
2003
).
The damping of LC opsin mRNA expression after 24 h of DD or LL may not be a
result of a run-down of the circadian oscillators that control opsin
expression. Rather, it may be due to un-couplings between the oscillator and
the biochemical machinery responsible for expression of LC mRNA. Dalal et al.
(2003) recently reported that
in Limulus eyes, the expression of opsin mRNA displayed robust
daynight rhythms when the animals were kept in normal LD conditions;
opsin mRNA concentrations was low at night and high in late afternoon and
early evening. This pattern of opsin mRNA expressions was regulated by light,
regardless whether the eye received circadian efferent input.
Dopamine plays modulatory roles in the visual system
(Baldridge et al., 1987;
Witkovsky and Dearry, 1992
; Ko
et al., 2003
,
2004
). Alfinito and
Townes-Anderson (2001
) reported
that in the retinas of tiger salamander, dopamine increased rod opsin mRNA
expression. They further demonstrated that the effect of dopamine on opsin
mRNA expression is mediated, via dopamine D4 receptors, by
cAMP-regulated protein kinase activities. In this study, we found that
dopamine exerts its role on red cone opsin mRNA expression via
D1 receptors in zebrafish. Interestingly, such an effect of
dopamine on LC opsin mRNA expression was seen only in the early morning. This
could be explained by several possibilities. First, dopamine activates
different types of receptors at different times in the day and night, which in
turn, triggers different intracellular signaling pathways. Previous studies
have shown that the effects of dopamine on photoreceptor cells or on inner
retinal neurons are mediated by different receptors
(Dearry and Burnside, 1986
;
Besharse et al., 1988
; Fan and
Yazulla, 1999
,
2001
). Ribelayga and Mangel
(2003
) recently revealed two
separate but parallel dopamine mechanisms that regulate horizontal cell
couplings in the goldfish retinas. Among those two pathways, one is mediated
by an endogenous circadian mechanism, and the other is controlled by light. In
dark-adapted retinas, under circadian control the release of vitreal dopamine
increased during the subjective day. This increase of vitreal dopamine is
sufficient to activate D2 receptors but not D1
receptors. Conversely, light produced larger effects on dopamine release than
the circadian clock. Under daylight, the release of vitreal dopamine further
increased, thereby, activating D1 receptors. Thus, dopamine may
function differently, via different receptor pathways, at different
times in the day and night.
The second possibility is that dopamine shifts the expression of early
circadian genes. Steenhard and Besharse
(2000) reported that in frog
retinas, per2 expression is acutely regulated by dopamine. In the
early morning, administration of dopamine increased per expression
threefold. The effect of dopamine on per expression can be mimicked
by light via a different intracellular signaling pathway. It has been
shown that functional expression of period plays a role in protein
kinase activity (Cermakian et al.,
2002
), which in turn, regulates opsin mRNA expression
(Cohen et al., 1992
;
Alfinito and Townes-Anderson,
2001
). The third possibility is that via cAMP pathways
dopamine regulates the circadian sensitivity of retinal photoreceptor cells.
Ko et al. (2003
) reported that
in chick retinas, brief dopamine treatment (15 min) decreased the affinity of
cGMP-gated channels on cone photoreceptor cells. This effect, however, was
seen only during the day but not during the night. The fourth possibility is
that dopamine cannot increase LC opsin mRNA expression in the evening because
at this circadian time the expression is near saturation levels.
Light produces effects on circadian rhythms of visual sensitivity. It was
unexpected, however, that prolonged light (>24 h) would result in decreased
LC opsin mRNA expression. We can preclude the possibility of light damage to
the retina due to prolonged light exposure, as histological sections revealed
no alternations in the structure of the outer or the inner retinas. In fact,
after 5 days of LL the absolute behavioral visual sensitivity is increased
(Li and Dowling, 1998).
In summary, we have demonstrated that in zebrafish the circadian rhythms of behavioral cone sensitivity correlate with daily fluctuations of cone opsin gene expression and photoreceptor outer segment optical density in the normal LD and the first 24 h of LL and DD. We have also demonstrated that circadian expression of opsin is influenced by dopamine. It is of particular interest that this effect is seen only in the early morning, when LC opsin mRNA expression is low.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alfinito, P. D. and Townes-Anderson, E. (2001). Dopamine D4 receptor-mediated regulation of rod opsin mRNA expression in tiger salamander. J. Neurochem. 76,881 -891.[CrossRef][Medline]
Allward, B. A. and Dowling, J. E. (2001). The pineal gland in wild-type and two zebrafish mutants with retinal defects. J. Neurocytol. 30,493 -501.[CrossRef][Medline]
Allward, B. A., Lall, A. B., Brockerhoff, S. E. and Dowling, J.
E. (2001). Synapse formation is arrested in retinal
photoreceptors of the zebrafish nrc mutant. J.
Neurosci. 21,2330
-2342.
Baldridge, W. H., Ball, A. K. and Miller, R. G. (1987). Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. J. Comp. Neurol. 265,428 -436.[CrossRef][Medline]
Barlow, R. B. (1983). Circadian rhythms in the Limulus visual system. J. Neurosci. 3, 856-870.[Abstract]
Barlow, R. B., Chamberlain, S. C. and Levinson, J. Z. (1980). The Limulum brain modulates the structure and function of the lateral eyes. Science 210,1037 -1039.[Medline]
Battelle, B. A. (1991). Regulation of retinal functions by octopaminergic efferent neurons in Limulus. Prog. Retinal Res. 10,335 -355.
Berson, D. M., Dunn, F. A. and Takao, M.
(2002). Phototransduction by retinal ganglion cells that set the
circadian clock. Science
295,1070
-1073.
Besharse, J. C., Spratt, G. and Reif-Lehrer, L. (1988). Effects of kynurenate and other excitatory amino acid antagonists as blockers of light- and kainate-induced retinal rod photoreceptor disc shedding. J. Comp. Neurol. 274,295 -303.[CrossRef][Medline]
Bassi, C. J. and Powers, M. K. (1986). Daily fluctuations in the detectability of dim lights by humans. Physiol. Behav. 38,871 -877.[CrossRef][Medline]
Bassi, C. J. and Powers, M. K. (1987). Circadian rhythm in goldfish visual sensitivity. Invest. Ophthalmol. Vis. Sci. 28,1811 -1815.[Abstract]
Bassi, C. J. and Powers, M. K. (1990). Shedding of rod outer segments is light-driven in goldfish. Invest. Ophthalmol. Vis. Sci. 31,2314 -2319.[Abstract]
Brockerhoff, S. E., Hurley, J. B., Niemi, G. A. and Dowling, J.
E. (1997). A new form of inherited red-blindness identified
in zebrafish. J. Neurosci.
17,4236
-4242.
Bruenner, U. and Burnside, B. (1986). Pigment granule migration in isolated cells of the teleost retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 27,1634 -1643.[Abstract]
Cahill, G. M. (1996). Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res. 708,177 -181.[CrossRef][Medline]
Cahill, G. M. and Besharse, J. C. (1991). Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light and D2 dopamine receptors. J. Neurosci. 11,2959 -2971.[Abstract]
Cahill, G. M. and Besharse, J. C. (1993). Circadian clock functions localized in Xenopus retinal photoreceptors. Neuron 10,573 -577.[Medline]
Cameron, D. A. (2002). Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Vis. Neurosci. 19,365 -372.[CrossRef][Medline]
Cermakian, N., Pando, M. P., Thompson, C. L., Pinchak, A. B., Selby, C. P., Gutierrez, L., Wells, D. E., Cahill, G. M., Sancar, A. and Sassone-Corsi, P. (2002). Light induction of a vertebrate clock gene involves signaling through blue-light receptors and MAP kinases. Curr. Biol. 12,844 -848.[CrossRef][Medline]
Chinen, A., Hamaoka, T., Yamada, Y. and Kawamura, S.
(2003). Gene duplication and spectral diversification of cone
visual pigments of zebrafish. Genetics
163,663
-675.
Cohen, A. I., Todd, R. D., Harmon, S. and O'Malley, K. L.
(1992). Photoreceptors of mouse retinas possess D4 receptors
coupled to adenylate cyclase. Proc. Natl. Acad. Sci.
USA 89,12093
-12097.
Dalal, J. S., Jinks, R. N., Cacciatore, C., Greenberg, R. M. and Battelle, B. A. (2003). Limulus opsins: diurnal regulation of expression. Vis. Neurosci. 20,523 -534.[CrossRef][Medline]
Dearry, A. and Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors. J. Neurochem. 46,1006 -1021.[Medline]
Dowling, J. E. (1987). The Retina: An Approachable Part of The Brain. Cambridge, MA: Harvard University Press.
Fan, S. F. and Yazulla, S. (1999). Modulation of voltage-dependent K+ currents (IK(V)) in retinal bipolar cells by ascorbate is mediated by dopamine D1 receptors. Vis. Neurosci. 16,923 -931.[CrossRef][Medline]
Fan, S. F. and Yazulla, S. (2001). Dopamine depletion with 6-OHDA enhances dopamine D1-receptor modulation of potassium currents in retinal bipolar cells. Vis. Neurosci. 18,327 -337.[CrossRef][Medline]
Forsell, J., Ekstrom, P., Flamarique, I. N. and Holmqvist, B. (2001). Expression of pineal ultraviolet- and green-like opsins in the pineal organ and retina of teleosts. J. Exp. Biol. 204,2517 -2525.[Medline]
Gooley, J. J., Lu, J., Fischer, D. and Saper, C. B.
(2003). A broad role for melanopsin in nonvisual photoreception.
J. Neurosci. 23,7093
-7106.
Gothilf, Y., Coon, S. L., Toyama, R., Chitnis, A., Namboodiri,
M. A. and Klein, D. C. (1999). Zebrafish serotonin
N-acetyltransferase-2: marker for development of pineal photoreceptors and
circadian clock function. Endocrinology
140,4895
-4903.
Gothilf, Y., Toyama, R., Coon, S. L., Du, S. J., Dawid, I. B. and Klein, D. C. (2002). Pineal-specific expression of green fluorescent protein under the control of the serotonin-N-acetyltransferase gene regulatory regions in transgenic zebrafish. Dev. Dyn. 225,241 -249.[CrossRef][Medline]
Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G. and Donner, K. (2000). In search of the visual pigment template. Vis. Neurosci. 17,509 -528.[CrossRef][Medline]
Green, C. B. and Besharse, J. C. (1996).
Identification of a novel vertebrate circadian clock-regulated gene encoding
the protein nocturnin. Proc. Natl. Acad. Sci. USA
93,14884
-14888.
Hattar, S., Liao, H. W., Takao, M,, Berson, D. M. and Yau, K.
Y. (2002). Melanopsin-containing retinal ganglion cells:
architecture, projections, and intrinsic photosensitivity.
Science 295,1065
-1070.
Hattar, S. et al. (2003). Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 76-81.[CrossRef][Medline]
Hawryshyn, C. W., Haimberger, T. J. and Deutschlander, M. E. (2001). Microspectrophotometric measurements of vertebrate photoreceptors using CCD-based detection technology. J. Exp. Biol. 204,2431 -2438.[Medline]
Hendrickson, A. E. and Kelly, D. E. (1971). Development of the amphibian pineal organ: fine structure during maturation. Anat. Rec. 170,129 -142.[Medline]
Jenkins, A., Munoz, M., Tarttelin, E. E., Bellingham, J., Foster, R. G. and Hankins, M. W. (2003). VA opsin, melanopsin, and an inherent light response within retinal interneurons. Curr. Biol. 13,1269 -1278.[CrossRef][Medline]
Kelly, D. E. and Smith, S. W. (1964). Fine
structures of the pineal organs of the adult frog, Rena pipiens. J.
Cell. Biol. 22,653
-674.
Ko, G. Y., Ko, M. L., Dryer, S. E. (2003).
Circadian phase-dependent modulation of cGMP-gated channels of cone
photoreceptors by dopamine and D2 agonist. J.
Neurosci. 23,3145
-3153.
Ko, G. Y., Ko, M. L., Dryer, S. E. (2004).
Circadian regulation of cGMP-gated channels of vertebrate cone photoreceptors:
role of cAMP and Ras. J. Neurosci.
24,1296
-1304.
Korenbrot, J. I. and Fernald, R. D. (1989). Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature 337,454 -457.[CrossRef][Medline]
LaVail, M. M. (1976). Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 194,1071 -1074.[Medline]
Li, L. (2001). Zebrafish mutants: behavioral genetic studies of visual system defects. Dev. Dyn. 221,365 -372.[CrossRef][Medline]
Li, L. and Dowling, J. E. (1997). A dominant
form of inherited retinal degeneration caused by a non-photoreceptor
cell-specific mutation. Proc. Natl. Acad. Sci. USA
94,11645
-11650.
Li, L. and Dowling, J. E. (1998). Zebrafish visual sensitivity is regulated by a circadian clock. Vis. Neurosci. 15,851 -857.[CrossRef][Medline]
Li, L. and Dowling, J. E. (2000). Effect of
dopamine depletion on visual sensitivity of zebrafish. J.
Neurosci. 20,1893
-1903.
Lin, Z. S. and Yazulla, S. (1994). Depletion of retinal dopamine increases brightness perception in goldfish. Vis. Neurosci. 11,683 -693.[Medline]
Maaswinkel, H. and Li, L. (2003). Olfactory
input increases visual sensitivity in zebrafish: a possible function for the
terminal nerve and dopaminergic interplexiform cells. J. Exp.
Biol. 206,2201
-2209.
Missale, C., Nash, S. R., Robinson, S. W., Jaber, M. and Caron,
M. G. (1998). Dopamine receptors: from structure to
functions. Physiol. Rev.
78,189
-225.
Morin, L. P., Blanchard, J. H. and Provencio, I. (2003). Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J. Comp. Neurol. 465,401 -416.[CrossRef][Medline]
Nawrocki, L., BreMiller, R., Streisinger, G. and Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Res. 25,1569 -1576.[CrossRef][Medline]
Pando, P. M., Pinchak, A. B., Cermakian, N. and Sassone-Corsi,
P. (2001). A cell-based system that recapitulates the dynamic
light-dependent regulation of the vertebrate clock. Proc. Natl.
Acad. Sci. USA 98,10178
-10183.
Pierce, M. E. and Besharse, J. C. (1985). Circadian regulation of retinomotor movements I. Interaction of melatonin and dopamine in the control of cone length. J. Gen. Physiol. 86,671 -689.[Abstract]
Pierce, M. E., Sheshberadaran, H., Zhang, Z., Fox, L. E., Applebury, M. L. and Takahashi, J. S. (1993). Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron 10,579 -584.[Medline]
Provencio, I., Jiang, G., DeGrip, W. J., Hayes, W. P. and
Rollag, M. D. (1998). Melanopsin: an opsin in melanophores,
brain and eye. Proc. Natl. Acad. Sci. USA
95,340
-345.
Pu, G. A. and Dowling, J. E. (1981). Anatomical
and physiological characteristics of pineal photoreceptor cell in the larval
lamprey, Petromyzon marinus. J. Neurophysiol.
46,1018
-1038.
Ren, J. Q. and Li, L. (2004). Rod and cone signaling transmission in the retina of zebrafish: an ERG study. Int. J. Neurosci. 114,259 -270.[CrossRef][Medline]
Ribelayga, C. and Mangel, S. C. (2003). Absence of circadian clock regulation of horizontal cell gap junctional coupling reveals two dopamine systems in the goldfish retina. J. Comp. Neurol. 467,243 -253.[CrossRef][Medline]
Robinson, J., Schmitt, E. A., Harosi, F. I., Reece, R. J. and
Dowling, J. E. (1993). Zebrafish ultraviolet visual pigment:
Absorption spectrum, sequence, and localization. Proc. Natl. Acad.
Sci. USA 90,6009
-6012.
Ruby, N. F., Brennan, T. J., Xie, X., Cao, V., Franken, P.,
Heller, H. C. and O'Hara, B. F. (2002). Role of melanopsin in
circadian responses to light. Science
298,2211
-2213.
Steenhard, B. M. and Besharse, J. C. (2000).
Phase shifting the retinal circadian clock: xPer2 mRNA induction by light and
dopamine. J. Neurosci.
20,8572
-8577.
Westerfield, M. (1995). The Zebrafish Book: A Guide for The Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
Whitmore, D., Foulkes, N. S., Strahle, U. and Sassone-Corsi, P. (1998). Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat. Neurosci. 1,701 -707.[CrossRef][Medline]
Whitmore, D., Foulkes, N. S. and Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404, 87-91.[CrossRef][Medline]
Wilson, S. W. and Easter, S. S. (1991). A
pioneering growth cone in the embryonic zebrafish. brain. Proc.
Natl. Acad. Sci. USA 88,2293
-2296.
Witkovsky, P. and Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Prog. Retinal Res. 11,247 -292.
Young, R. W. (1967). The renewal of
photoreceptor cell outer segments. J. Cell. Biol.
33, 61-72.