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First published online October 19, 2007
Journal of Experimental Biology 210, 3821-3829 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007161
Immunohistochemical characterization of a parapinopsin-containing photoreceptor cell involved in the ultraviolet/green discrimination in the pineal organ of the river lamprey Lethenteron japonicum
1 Graduate School of Humanities and Sciences, Nara Women's University, Nara
630-8506, Japan
2 Department of Biology and Geosciences, Graduate School of Science, Osaka
City University, Osaka 558-8585, Japan
3 Core Research for Evolutional Science and Technology (CREST), Japan
Science and Technology Corporation, Kyoto 606-8502, Japan
4 Department of Biophysics, Graduate School of Science, Kyoto University,
Kyoto 606-8502, Japan
5 Nara Saho College, Nara 630-8566, Japan
* Authors for correspondence (e-mails: terakita{at}sci.osaka-cu.ac.jp; tamotsu{at}cc.nara-wu.ac.jp)
Accepted 16 August 2007
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Summary |
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Key words: pineal organ, parapinopsin, rhodopsin, ganglion cell, antagonistic chromatic response
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Introduction |
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;
Gaston and Menaker, 1968;
Morita et al., 1992;
Reiter, 1993). The pineal
organ is widely accepted as a synthesizer and secretor of melatonin
(Falcon et al., 1989;
Gern and Greenhouse, 1988;
Samejima et al., 2000;
Samejima et al., 1997;
Underwood, 1985). In addition
to the secretory response, the pineal photoreceptor transduces a light signal
to an electrical response, which is transmitted to the brain via pineal
ganglion cells (Dodt, 1973;
Dodt and Heerd, 1962;
Morita, 1969).
Physiologically, the pineal organ has two types of ganglion cell, chromatic
and achromatic. Several electrophysiological studies have demonstrated that
the neural activity of chromatic-type ganglion cells is inhibited by UV/short
wavelength light and excited by green/long wavelength light, whereas that of
achromatic-type ganglion cells is inhibited by visible light in the pineal
organ of the lamprey (Morita and Dodt,
1973), teleost (Morita,
1966) and frog (Dodt and Heerd,
1962). Therefore, chromatic-type ganglion cells detect the ratio
of short wavelength light to long wavelength light in environmental light
(Dodt, 1973), suggesting that
the pineal organ is involved in the wavelength discrimination of the photic
component in incident light.
The river lamprey Lethenteron japonicum also has a well-developed
photosensory pineal organ, in which some ganglion cells exhibit antagonistic
chromatic responses, in addition to a large number of achromatic-type ganglion
cells (Morita et al., 1989;
Uchida and Morita, 1994).
Electrophysiological studies have identified two types of photoreceptor cell
in the pineal organ, UV- and green-sensitive photoreceptor cells (hereafter
referred to as UV and green photoreceptor cells, respectively), both of which
hyperpolarize in response to light stimuli
(Tamotsu and Morita, 1986;
Uchida and Morita, 1990). The
sensitivity curve of green photoreceptor cells fits that of achromatic-type
ganglion cells with maximum sensitivity at 525 nm
(Uchida et al., 1992) but does
not fit that of chromatic-type ganglion cells with maximum sensitivity at 540
nm (Uchida and Morita, 1994).
We found that the lamprey rhodopsin with an absorption maximum at 
520 nm
(Hisatomi et al., 1997) (M.
Koyanagi, E. Kawano-Yamashita, Y. Kinugawa, T. Oishi, Y. Shichida, S. Tamotsu
and A. Terakita, unpublished observations) is expressed in a large number of
pineal photoreceptor cells (Koyanagi et
al., 2004). Taken together, these results suggest that green
photoreceptor cells containing lamprey rhodopsin achieve achromatic responses,
whereas green/long wavelength photoreceptor cells responsible for the
antagonistic chromatic response remain to be clarified. On the other hand, it
has been suggested that UV photoreceptor cells are responsible for the
antagonistic chromatic response but not for the achromatic response, based on
the sensitivity curves of the two types of ganglion cell.
Recently, we found the UV pigment lamprey parapinopsin in the lamprey
pineal organ (Koyanagi et al.,
2004). Lamprey parapinopsin is distinct from vertebrate cone and
rod opsins, and has a bistable nature as it exhibits photointerconversion by
UV and green light (Koyanagi et al.,
2004). Lamprey parapinopsin underlies a unique characteristic of
photoreceptor cells that differs from that of lamprey rhodopsin-containing
photoreceptor cells.
To understand the neural connections that generate the antagonistic
chromatic response, an effective strategy is to investigate how UV light
signals are transmitted to chromatic-type ganglion cells, because the
green/long wavelength photoreceptor cells responsible for the antagonistic
chromatic response have not been identified. In this study, we carried out
histological characterization of the lamprey parapinopsin-containing cells
involved in generating the antagonistic chromatic response and compared it
with that of the lamprey rhodopsin-containing cells, most of which generate
the achromatic response. Lamprey parapinopsin is expressed in the dorsal
region of the pineal organ, whereas lamprey rhodopsin is expressed in the
ventral region as revealed by in situ hybridization analysis
(Koyanagi et al., 2004), which
showed that UV photoreceptor cells and green photoreceptor cells are
distributed in the dorsal and ventral layer of the pineal organ, respectively.
We elucidated the structural characteristics and localization of UV
photoreceptor cells containing lamprey parapinopsin in detail by using an
antibody against lamprey parapinopsin, and compared them with those of lamprey
rhodopsin-containing cells. Furthermore, we histologically showed that the
light information from UV photoreceptor cells is directly transmitted to
ganglion cells.
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Materials and methods |
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Reverse transcription (RT)-PCR
Total RNA from the pineal organ, retina and brain was reverse transcribed
to cDNA using an oligo(dT) primer and Superscript III (Invitrogen, Carlsbad,
CA, USA), and the cDNAs were used as templates for PCR amplification. To
obtain an internal standard for normalizing expression levels of the lamprey
parapinopsin (AB116380; all accession nos are for GenBank/EMBL/DDBJ) and the
lamprey rhodopsin (AB116382), we cloned glyceraldehyde 3-phosphate
dehydrogenase (GAPDH, AB300852), a housekeeping gene, from lamprey with
degenerate primers; forward: 5'-CCIISIGCIGAYGCNCCNATGTT-3',
reverse: 5'-GTAICCRHAYTCRTTRTCRTACCA-3'. Gene-specific PCR
amplifications were performed with the following primer pairs:
5'-ACGTGTCGTACATTACGAGC-3' and
5'-TCACCACGATCATGGCGAAG-3' for lamprey parapinopsin;
5'-ACGAGTCGTACGTAGTCTAC-3' and
5'-GTGAAGATGTAGAAGGCCAC-3' for lamprey rhodopsin;
5'-ACGACAACTTCGTGATCCTG-3' and
5'-CTTCCTTCACCTTAGCCTTG-3' for GAPDH. The optimal annealing
temperature was 60°C for the lamprey parapinopsin and GAPDH primer pairs,
and 65°C for the lamprey rhodopsin primer pairs.
Generation of anti-lamprey parapinopsin and anti-lamprey rhodopsin antibodies
The anti-lamprey parapinopsin and anti-lamprey rhodopsin antibodies were
generated as reported previously (Koyanagi
et al., 2005), with the following modifications. The 50 amino
acids of the C-terminal region of the lamprey parapinopsin
(Met324–Ser373) and the 47 amino acids of the C-terminal region of the
lamprey rhodopsin (Ile307–Ala353) were fused to maltose-binding protein
in the expression vector pMAL-c2X (New England Biolabs, Ipswich, MA, USA). The
fusion proteins were expressed in Escherichia coli and purified by
amylose affinity column chromatography (New England Biolabs). JW/CSK female
rabbits or BALB/c female mice were immunized four to six times with the
purified fusion proteins of lamprey parapinopsin and lamprey rhodopsin,
respectively.
Immunohistochemistry
Animals were quickly decapitated and their pineal organs were isolated with
a small piece of adjacent tissue. The pineal organs were fixed in Zamboni's
fixative [4% paraformaldehyde in 0.1 mol l–1 sodium phosphate
buffer (PB) containing 0.2% picric acid, pH 7.4] overnight at 4°C. Each
organ was cryoprotected by immersion in 0.1 mol l–1 PB
containing increasing concentrations of sucrose (15 and 30%), and embedded in
OCT compound (Sakura, Tokyo, Japan). Frozen sections (thickness: 15–30
µm) were prepared using a cryostat (Bright Instrument Co. Ltd, Huntingdon,
Cambridgeshire, UK), and mounted on 0.5% gelatin-coated slides.
Immunohistochemical analyses were conducted as reported previously
(Kawano et al., 2006). In
brief, the sections were incubated overnight at 4°C with primary rabbit
antiserum against lamprey parapinopsin [diluted 1:1000 in 0.1 mol
l–1 phosphate-buffered saline (PBS, pH 7.4) containing 0.3%
Triton X-100 (PBS-T) and 1% bovine serum albumin], and subsequently incubated
with Alexa 488-conjugated anti-rabbit IgG (diluted 1:500 in PBS-T; Molecular
Probes, Eugene, OR, USA) for 5 h at room temperature. In the
double-immunostaining experiment, sections were incubated overnight at 4°C
with the first primary rabbit antiserum against lamprey parapinopsin (diluted
1:1000 in PBS-T containing 1% bovine serum albumin) and subsequently incubated
with Alexa 488-conjugated anti-rabbit IgG (diluted 1:500 in PBS-T) for 5 h at
room temperature. The same sections were then incubated with the second
primary mouse antiserum against the lamprey rhodopsin (diluted 1:1000 in PBS-T
containing 1% bovine serum albumin) overnight at 4°C, and subsequently
incubated with Alexa 594-conjugated anti-mouse IgG (diluted 1:500 in PBS-T;
Molecular Probes) for 5 h at room temperature.
For the whole-mount analysis, the dorsal region was dissected from the fixed pineal organs. The specimens were incubated with the primary rabbit antiserum against lamprey parapinopsin (diluted 1:1000 in PBS-T containing 1% bovine serum albumin and sodium azide) for 5 days at 4°C, and then with Alexa 488-conjugated anti-rabbit IgG (diluted 1:500 in PBS-T containing sodium azide) for 5 days at 4°C.
To confirm the specificity of the antisera against lamprey parapinopsin and lamprey rhodopsin, sections were incubated in rabbit or mouse normal serum (diluted 1:250 in PBS-T containing 1% bovine serum albumin) instead of the primary antisera. For control staining of lamprey parapinopsin, both the antigen (lamprey parapinopsin peptide) and the antiserum against lamprey parapinopsin were first mixed and incubated overnight at 4°C. Control sections were then incubated in the primary antiserum absorbed by lamprey parapinopsin. In all control preparations, no immunoreactivity was observed.
Intracellular injection of the dye into the UV photoreceptor cells
The removed pineal organ with a piece of adjacent tissue was placed in a
recording chamber and perfused with oxygenated Ringer solution under dark
adaptation for at least 30 min. Intracellular recording was carried out with a
glass microelectrode filled with 2% neurobiotin (Vector Laboratories,
Burlingame, CA, USA) in 1 mol l–1 KCl, with a resistance
range from 120 to 200 M
. Responses were amplified by a high-input
impedance amplifier (IR-183, Cygnus Technology, Delaware, PA, USA). After the
UV-sensitive photoresponse had been confirmed, intracellular injections of
neurobiotin were performed by passing 2–5 nA depolarizing rectangular
pulses of 200 ms duration at 2 Hz for about 3 min. The pineal organ was fixed
with 4% paraformaldehyde in 0.1 mol l–1 PB, and frozen
sections (thickness: 30 µm) were obtained using a cryostat. Visualization
of the injected cells was achieved with Alexa 568-conjugated streptavidin
(Molecular Probes).
Electron microscopy
The pineal organs were fixed by immersion in 2.5% glutaraldehyde prepared
with 0.1 mol l–1 PB. After the specimens had been washed in
PBS, they were postfixed with 1% OsO4 in 0.1 mol
l–1 PB for 1 h, dehydrated in a graded series of alcohol, and
embedded in epoxy resin (Quetol 812, Nisshin EM, Tokyo, Japan). Semi-thin and
ultrathin sections were made using an ultramicrotome (EM-UC6, Lieca,
Heidelberg, Germany). Semi-thin sections were stained with a mixture of
azur-II and toluidine blue for light-microscopic observation. Ultrathin
sections were stained with uranyl acetate and lead citrate, and examined with
an electron microscope (JEM 1220, JEOL, Tokyo, Japan).
For immunoelectron microscopy, the pineal organs were fixed in Zamboni's fixative including 0.05% glutaraldehyde for 2 h, and kept in Zamboni's fixative. After washing in PBS, the specimens were incubated for 1 week at 4°C with anti-lamprey parapinopsin antiserum (diluted 1:1000 in PBS) and rinsed with PBS. The specimens were incubated with biotin-labelled anti-rabbit IgG (diluted 1:1000 in PBS; Biosource, Camarillo, CA, USA) and rinsed with PBS, then incubated with horseradish peroxidase-labelled streptavidin (diluted 1:250 in PBS; ICN, Aurora, OH, USA) and rinsed with PBS. Alternatively, the specimens were incubated with horseradish peroxidase-labelled anti-rabbit IgG (diluted 1:1000 in PBS; Biosource) and rinsed with PBS. To visualize the immunoreaction, the specimens were incubated with 0.025% diaminobenzidine (DAB; Sigma, St Louis, MO, USA) in 0.05 mol l–1 Tris-HCl (pH 7.4) with 0.03% H2O2 for 10–20 min. The specimens were postfixed with 1% OsO4 in 0.1 mol l–1 PB for 1 h at room temperature, dehydrated in a graded series of ethanol, and embedded in epoxy resin (Quetol 812). Ultrathin sections were prepared, stained with uranyl acetate and lead citrate, and examined with an electron microscope.
Retrograde labelling
Retrograde labelling was carried out as described previously
(Samejima et al., 1989) with
the following modifications. After decapitation of the lamprey, the intact
brains were carefully removed and transferred into oxygenated lamprey Ringer
solution (138.6 mmol l–1 NaCl, 2.82 mmol l–1
KCl, 0.24 mmol l–1 NaHCO3, 2.07 mmol
l–1 CaCl2 in distilled water). The pineal tract
was transected 2–3 mm away from the pineal organ using a pair of
microscissors, and crystals of a neural tracer (neurobiotin) were applied to
the cut region. After 30 min, excess tracer was rinsed away with Ringer
solution, and the brain was incubated overnight at 4°C in oxygenated
Ringer solution. After incubation, the brains were fixed in Zamboni's fixative
overnight at 4°C and sectioned with a cryostat. To visualize the neural
tracer, the sections were incubated with Alexa 594-conjugated streptavidin for
5 h at room temperature. Additionally, immunohistochemistry was performed as
described above for the immunofluorescent detection of lamprey
parapinopsin.
For the control experiment, neural tracer crystals were applied to the surface of the pineal stalk in the intact brain without cutting. In the control sections, ganglion cells were not labelled, confirming that the ganglion cells were retrogradely labelled from the pineal stalk (data not shown).
We examined the stained sections under a fluorescence microscope (BX51, Olympus, Tokyo, Japan) and a confocal laser-scanning microscope (TCS-NT, Leica, Bansheim, Germany).
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). In brief, serial confocal images were taken by serial
optical sectioning using a confocal laser-scanning microscope.
Three-dimensional images were reconstructed from these serial confocal images
by means of a volume-rendering method with reconstruction software (VoxelView;
Vital Image, Minneapolis, MN, USA). |
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We then prepared serial sections across the rostro-caudal axis and immunohistochemically investigated the distribution of photoreceptor cells. Typical results are shown in Fig. 4. In the cross-section around the peripheral portion, a larger number of lamprey parapinopsin-containing cells than lamprey rhodopsin-containing cells were observed (Fig. 4B). On the other hand, a larger number of lamprey rhodopsin-containing cells were observed in the cross-section around the central portion (Fig. 4C). Immunohistochemical observations of the pineal organ through the rostro-caudal axis revealed that lamprey parapinopsin-containing cells were more abundant in the peripheral portion than in the central portion.
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). We
therefore investigated the details of the connections between lamprey
parapinopsin-containing cells in a wide area, by using the anti-parapinopsin
antibody. The confocal images revealed that some lamprey
parapinopsin-containing cells were connected with each other in the basal
processes and formed a neuropile that spread across a wide area, at least
about 250 µm x 100 µm (indicated in
Fig. 5B), in the whole-mount
specimens of the dorsal and peripheral portion
(Fig. 5A,B).
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) but not its achromatic response
(Uchida et al., 1992). In this
study, we therefore histologically characterized lamprey
parapinopsin-containing cells and their connection to ganglion cells in order
to find out the details of the antagonistic chromatic response.
We investigated the expression pattern of lamprey parapinopsin in the
pineal organ, retina and brain with RT-PCR analysis. This demonstrated that
lamprey parapinopsin functions only in the pineal organ
(Fig. 1), suggesting that
lamprey parapinopsin is responsible for only the pineal UV reception. In
contrast, our results and previous reports
(Tamotsu et al., 1990;
Tamotsu et al., 1994)
demonstrated that lamprey rhodopsin functions in both the pineal organ and the
retina (Fig. 1), showing that
lamprey rhodopsin is responsible for both visual and non-visual
photoreception. In the brain, immunoreactivity against the rod and cone opsins
has been shown in three species of lamprey, Petromyzon marinus, Lampetra
fluviatilis and Ichthyomyzon unicuspis
(Garcia-Fernandez et al.,
1997). Since neither the lamprey parapinopsin nor the lamprey
rhodopsin gene was expressed in the brain in this study
(Fig. 1), photopigments other
than lamprey parapinopsin and lamprey rhodopsin would be expressed in the
brain of Lethenteron japonicum.
In the present study, we immunohistochemically investigated the
distribution of lamprey parapinopsin in order to identify a specific
UV-receptive region in the pineal organ. Our results showed that lamprey
parapinopsin is localized in not only the dorsal region but also the
peripheral region, which is the dorso-ventral border region of the pineal
organ (Fig. 2A,
Fig. 3A). The number of lamprey
parapinopsin-containing cells is greater around the peripheral portion than in
the central portion (Fig. 4).
In a previous study, many responses of chromatic-type ganglion cells were
recorded in the peripheral portion of the pineal organ
(Uchida and Morita, 1994).
These facts indicate the possibility that, in the peripheral portion, light
information from lamprey parapinopsin-containing cells is transmitted to
chromatic-type ganglion cells. Double immunostaining showed that lamprey
parapinopsin and lamprey rhodopsin are distributed mainly in the dorsal and
ventral layer of the pineal organ, respectively
(Fig. 3A,B), which is
consistent with previous in situ hybridization results
(Koyanagi et al., 2004).
Remarkably, our confocal images revealed for the first time that each
photoreceptor cell in the peripheral portion contains either lamprey
parapinopsin or lamprey rhodopsin; in other words, the two pigments are never
colocalized in a photoreceptor cell even in the peripheral region
(Fig. 3C,D). These results
suggest that UV light information for the inhibitory response and green/long
wavelength light information for the excitatory response project to chromatic
ganglion cells in the peripheral portion.
Our previous studies demonstrated that lamprey parapinopsin has molecular
properties quite different from those of vertebrate visual pigments
(Koyanagi et al., 2004). It is
considered that the molecular properties are possibly related to the
functional characteristics of photoreceptor cells, and it is therefore
interesting to compare the fine structures of the functional parts, the outer
segment and the synaptic ribbon between photoreceptor cells, containing
distinct photopigments, lamprey parapinopsin and lamprey rhodopsin. The outer
segment of dorsal photoreceptor cells, which contains lamprey parapinopsin
(Fig. 6B), has a cap-like
structure, similar to that of pineal photoreceptor cells in the ventral region
(Fig. 6C)
(Collin, 1971;
Pu and Dowling, 1981). We have
already found electrophysiologically that dorsal photoreceptor cells
containing lamprey parapinopsin are the UV-sensitive cells
(Koyanagi et al., 2004). Most
of the dorsal photoreceptor cells showed lamprey parapinopsin immunoreactivity
in the pineal organ (Fig. 2A,
Fig. 3A), and the synaptic
ribbon existed in the basal processes of the dorsal photoreceptor cells
(Fig. 6D), as in the ventral
photoreceptor cells (Fig. 6E).
These features suggest that lamprey parapinopsin-containing UV photoreceptor
cells have a structure similar to that of lamprey rhodopsin-containing
photoreceptor cells in both input and output light information parts, although
lamprey parapinopsin has molecular properties distinct from those of the
visual pigment lamprey rhodopsin.
We previously found the existence of dye coupling, which indicates cell
connection through the gap junction, in the basal processes of UV
photoreceptor cells by intracellular injection
(Koyanagi et al., 2004). In
the present study, the finding was reconfirmed
(Fig. 5A, inset) and,
furthermore, most of the lamprey parapinopsin-containing cells contacted each
other in the dorsal and peripheral portion. These results suggest that UV
photoreceptors form a wide neural network, at least 250 µm x 100
µm in area (Fig. 5B). These
histological characteristics of lamprey parapinopsin-containing cells are
important for speculating on the properties of pineal UV reception and neural
projection to chromatic-type ganglion cells. The UV photoreceptor cells are
connected with each other, and make a large photoreceptive field. Accordingly,
UV photoreceptor cells can average the UV light information reaching the
pineal organ by cancelling the effect of shade. On the other hand, in the case
of green light photoreceptor cells containing lamprey rhodopsin, the existence
of dye coupling like that in UV photoreceptor cells could not be found by
intracellular injection into a single photoreceptor cell (E.K.-Y., A.T., M.K.,
Y.S., T.O. and S.T., unpublished observations).
Most ganglion cells were localized in the ventral and peripheral regions,
whilst a few were localized in the dorsal region
(Fig. 7). This localization
profile of the ganglion cells was different from that of the lamprey
parapinopsin-containing cells (Fig.
2A, Fig. 3A),
suggesting that they may not be directly connected. However, in this study, we
found that lamprey parapinopsin-containing cells form a wide neural network
(Fig. 5), and almost all the
basal processes from the lamprey parapinopsin-containing cells were in direct
contact with the ganglion cells in the peripheral region
(Fig. 8). These results suggest
that the ganglion cells of the peripheral portion receive UV light information
that is converged in the UV photoreceptor layer in the pineal organ, and
achieve the antagonistic chromatic response. In the electrophysiological study
of the pike pineal, slow potentials that originated in the photoreceptor cells
were recorded from all parts of the pineal organ, while ganglion cells were
scarce in the distal part and absent in the medial one
(Falcon and Meissl, 1981).
Moreover, the interconnections between photoreceptor cells were demonstrated
in some fish – rainbow trout
(Ekström and Meissl, 1988)
and ayu (Omura, 1984).
Possibly, a similar network to the lamprey UV photoreceptor cells may be
present in the pineal organ of the teleost, too.
In chromatic-type ganglion cells, neural firing is inhibited and excited by
UV and green/long wavelength light, respectively
(Uchida and Morita, 1994). UV
photoreceptor cells show hyperpolarizing responses to light
(Koyanagi et al., 2004;
Uchida and Morita, 1990). Our
results demonstrate that chromatic-type ganglion cells directly receive UV
light information from lamprey parapinopsin-containing cells. This suggests
that the hyperpolarization of UV photoreceptor cells causes suppression of the
release of excitatory transmitters, such as glutamate, and produces the
subsequent inhibitory responses of chromatic-type ganglion cells, just as
phototransduction does in retinal photoreceptor cells. However, it remains
unclear whether the pineal photoreceptor cells that are involved in the
excitatory response to green/long wavelength light are depolarized by light
stimulation or indirectly connect with chromatic-type ganglion cells via an
interneuron. We have not found the neural connection between lamprey
rhodopsin-containing cells and chromatic-type ganglion cells. The maximum
sensitivities of the excitatory responses were reported to be 540 nm
(Uchida and Morita, 1994),
which does not fit the absorption maximum of lamprey rhodopsin (M. Koyanagi,
E. Kawano-Yamashita, Y. Kinugawa, T. Oishi, Y. Shichida, S. Tamotsu and A.
Terakita, unpublished observations)
(Hisatomi et al., 1997).
Therefore, there is the possibility that an unknown photopigment contained in
photoreceptor cells is involved in the excitatory response. It would be of
interest to study how the excitatory response to green/long wavelength light
is produced in the pineal organ.
The antagonistic chromatic response has also been found in the pineal
complexes of lower vertebrates, such as fish and frogs
(Dodt and Heerd, 1962;
Morita, 1966). We have already
isolated the lamprey parapinopsin homologues from rainbow trout and clawed
frog pineal complexes (Koyanagi et al.,
2004). Parapinopsin possibly generates the antagonistic chromatic
response for pineal UV reception in the vertebrate. Therefore, the mechanism
of the antagonistic chromatic response could be elucidated by investigating UV
photoreceptor cells, using parapinopsin as a marker.
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Acknowledgments |
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References |
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