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OCR for page 19
Cone Visual Pigments in
Monkeys and Humans
JAM ES K. BOWMAKER
Color vision in humans is based on three spectrally different classes
of photoreceptors, that is, three classes of cones containing different visual
pigments. The absorbance spectra of these different pigments were first es-
tablished by direct microspectrophotometric measurements from individual
cones by Marks et al. in 1964. Their data, along with the data of Brown
and Wald (1964), showed the expected clear evidence for three types of
cones with maximum absorbance, Ama=' at about 560, 530, and 440 to 460
nm. Since then various attempts have been made to establish with more
precision the Oman and the shape of the absorbance spectra of the three
pigments in humans (Dartnall et al., 1983) and to compare them with those
found in Old World monkeys (Bowmaker et al., 1983; MacNichol et al.,
1983~. The visual pigments of New World monkeys have also been inves-
tigated and correlated with the marked variations in color vision found in
these species (e.g., Mollon et al., 1984b).
This paper reviews the present position, as determined from microspec-
trophotometry, and addresses the following questions: How many visual
pigments are available to primates? Are there spectrally preferred posi-
tions for the pigments? If so, can they be related to anomalous pigments
in humans? In addition, some controversy has arisen as to the spectral
location of short-wave receptors in primates (Mansfield et al., 1984), and
I shall present further evidence from both Old and New World monkeys
suggesting differences between species.
Microspectrophotometric recording from primate photoreceptors is
difficult: the cone outer segments are small, with diameters of only 1 to 2
~m, and they break down structurally within a relatively short time. Thus,
the transverse absorbance spectra recorded from them have maximum
densities of only about 0.015 to 0.020 with low signal-to-noise ratios. (For
19
OCR for page 20
20
JAMES K BOWMAKER
a review see MacNichol et al., 1983~. In analyzing the data we set rigid
criteria by which to select records from individual cones and then estimate
the Oman by fitting a template curse to the absorbance spectrum (see Mollon
et al., 1984, for details). Ideally, the template curve should be expressed in
such a way that it remains constant in shape when displaced throughout the
spectrum, and my co-workers and I have previously found that the Dartnall
nomogram (based on frog rhodopsin with Max at 502 nm) expressed
on a scale of >~/4 iS a reasonable approximation (Barlow, 1982; Mollon
et al., 1984b). More recently, Mansfield (1985) and MacNichol (1986)
have demonstrated that a transformation to F/Fmax (frequency/frequency
maximum) produces a better fit to experimental data, and we have adopted
this template in the analysis of all the data presented here. The difference
in the Max determined from the two different templates is of course zero
near 500 nm (both based on frog rhodopsin), but it increases to about 2
nm at 565 nm, with the F/Fmax value being the shorter, since at longer
wavelengths the transformation, when expressed on a wavelength basis,
yields a slightly broader curve than the >~/4 transformation.
LONG- TO MIDDLE-WAVE PIGMENTS
Old World Monkeys and Humans
The cone pigments in macaques are well established. It is clear that
the two pigments in the red-green spectral region have Max at about
565 and 535 nm (Bowmaker et al., 1983; MacNichol et al., 1983~. We
have now had the opportunity to look at three other groups of Old World
primates: the baboon, Papio papio (Bowmaker et al., 1983), and two
types of guenon, the talapo~n, Cercopithecus (Miopithecus) talapoin, and
the moustached guenon, Cercopithecus cephus. These species extend the
range of platyrrhines studied. In addition, C. cephus is of particular interest
because of its facial coloration. The moustached guenon, or blue-faced
monkey, is characterized by a strikingly blue face surrounded by yellow
hair, and we hoped, perhaps naively, that its retina would have a somewhat
higher concentration of short-wave cones. We were fortunate in obtaining
data from six such cones, about 10 percent of the total, more than double
the numbers we have recorded from other species (Table 1~.
It is clear from Figure 1 that the distributions of cones in the four
species of Old World primates are similar and that the mean Oman for the
long-wave cones and that for the middle-wave cones are almost identical,
with overall means of 565.2 and 535.1 nm (Table 1~. The one rhesus
monkey listed in the present data yielded relatively few long-wave cones
with a mean Oman at about 562 nm, but our earlier data (Bowmaker et al.,
1983) suggest a Oman closer to 565 nm.
OCR for page 21
CONE VISUAL PIGMENTS IN MONKEYS AND HUMANS
12
4
12
4
12
.~' 1 2
z 4
20
12
4
l
~ ILL
PA
TA
MG
l
RH
Total
530 550 570
Wavelength nm
21
FIGURE 1 Distribution of values of peak sensitivity of indiviual cones (maximally sensitive
in the red-green spectral range) from four species of Old World primates: PA, Papio papio
(baboon) (four animals); TA, Cercopithecus talapoin (talapoin); MG, Cercopithecus cephus
(moustached guenon); and RH, Macaca mulatta (rhesus). The bottom panel is a summary
histogram of the four species.
OCR for page 22
22
TABLE 1 Old World Primate Visual Pigments ~ n nm)
JAMES K BOWMAKER
Short-wave
Middle-wave
Long-wave
Macaca mulatta 432.8 + 4.7 534.6 + 3.1 561.5 + 2.1
(Rhesus) (1) (1) (14) (7)
Cercopithecus 430.5 + 2.2 533.0 + 1.1 566.5 + 1.4
cephus (1) (6) (23) (18)
Cercopithecus 430.1 + 2.5 534.3 + 1.3 566.1 + 2.3
talapoin (1) (2) (23) (12)
Papio papio 428.5 + 3.3 536.4 + 1.2 564.5 + 1.2
(baboon) (4) (4) (40) (30)
Total Old 430.9 + 0.9 535.1 + 0.5 565.2 + 0.9
World (7) (13) (100) (67)
Human 419.0 + 2.1 531.4 + 0.7 563.7 + 0.6
(5) (4) (71) (102)
NOTE: Numbers in parentheses are either numbers of animals or numbers of cells
analyzed. Max values are + S.D.
Are the cone pigments in humans similar to those in Old World pri-
mates? We have recently made measurements from another five human
eyes enucleated because of melanoma; the distributions of the long- and
middle-wave cones are shown in Figure 2. These distributions are remark-
ably similar to those of the Old World primates, with mean Oman of 563.7
and 531.4 nm Table 1~: a similarity reflected in the spectral sensitivity mea-
surements obtained from suction electrode techniques both in macaques
(Baylor et al., 1987) and in humans (Schnapf et al., 1987~. The bimodality
in the populations of both long- and middle-wave cones suggested in our
earlier data from human eyes (Dartnall et al., 1983) was not apparent in
the present study.
A difference that is apparent between Old World monkeys and humans,
however, is the ratio of long- to middle-wave cones. In each of the four
species of Old World primates, there are fewer long-wave cones with an
overall ratio of 0.77 (101:131), whereas in the human data the situation is
reversed, with a ratio of long to middle of 1.67 (164:98~. These ratios are
based on the total number of cells identified, not the numbers of records
that passed our criteria, as listed in Able 1. Similar ratios were found in
our earlier studies: 0.73 for macaques (Bowmaker et al., 1983) and 1.3
for humans (Dartnall et al., 1983~. [The ratios given by Boynton (1988,
Table 1) are incorrect: he reversed our numbers of long- and middle-wave
cones.] In their suction electrode measurements of macaque foveal cones,
Baylor et al. (1987) found a ratio closer to 1.0 with 192 long-wave cones
and 211 middle-wave cones. It is not clear whether the difference we found
OCR for page 23
CONE VISUAL PIGMENTS IN MONKEYS AND HUMANS
12
4
4
4
28
20
12
H15
i
H13
H10
4
4
i L
H14
H12
t ~
Total
530 550 570
Wavelength rim
23
FIGURE 2 Distribution of values of peak sensitivity of individual cones (maximally
sensitive in the red-green spectral range) from the eyes of five persons. The bottom panel
is a summary histogram of the five individuals.
OCR for page 24
24
JAMES K BOWM'9KER
between Old World monkeys and humans is real or simply the result of
sampling biases.
New World Monkeys
The cone pigments present in New World monkeys are markedly
different from those of Old World monkeys, for New World monkeys
show a striking polymorphism of visual pigments maximally sensitive in the
red-green spectral region. This first became apparent in studies of color
vision in the squirrel monkey, Saimi?~ sciureus (Jacobs et al., 1981~. It is
now clear that this species has three pigments available in the middle to
long wavelengths with Oman (determined from microspectrophotometry) at
about 536, 550, and 563 nm (Mollon et al., 1984b). The pigments with
Oman at about 536 and 563 nm are very similar in spectral location to those
of Old World monkeys, but the P550 appears to be unique to New World
species.
The cone pigment complement in squirrel monkeys varies between
individuals such that all males possess only one pigment in the red-green
spectral region. This, combined with a short-wave pigment (see below),
allows the animal only dichromatic color vision (Mollon et al., 1984b).
However, the single pigment in the middle- to long-wave region may be
any one of the three available to the species. In the females the position is
more complex in that some animals are dichromats, resembling the males,
whereas others enjoy trichromacy and possess, in addition to the short-
wave pigment, a combination of any two of the three available longer-wave
pigments (13owmaker et al., 1985, 1987~. The polymorphism of pigments
and the resulting variation in color vision between individuals can be
explained by a genetic model (Mollon et al., 1984b; Jacobs and Neitz,
1985) that is distinctly different from that proposed for the inheritance of
color vision in humans and, by inference, in all Old World primates. The
model postulates that
there is only one genetic locus for a pigment in the red-green
spectral range;
· there are three alleles that can occur at the locus, the three al-
leles corresponding to the three slightly different opsins of the
photopigments;
· the locus is on the X-chromosome; and
· in those females that are heterozygous at the locus, only one of the
two alleles is expressed, owing to Lyonization or X-chromosome
inactivation, so that only one pigment is manufactured in any one
ce11.
OCR for page 25
CONE VISUAL PIGMENTS IN MONKEYS AND HUMANS
25
The polymorphism expressed in squirrel monkeys is not unique to the
cebid monkeys. It occurs in a similar form in the other major group of
New World monkeys- the callitrichids (Travis et al., 1985; Jacobs et al.,
1987~. In the common marmoset, Callithr~c jacchus jacchus, three pigments
are available in the red-green spectral region, but these are different from
those in Saimiri, with Oman at about 543, 557, and 564 nm Travis et al.,
1988~. The P564 is again similar to the long-wave pigment in Old World
monkeys, but the two pigments at shorter wavelengths are not common
to Old World species, although there are reports of cones from macaques
containing a pigment with Oman; at about 543 nm (Bowmaker et al., 1978;
MacNichol et al., 1983~. As with Saimir`, it appears that all males are
dichromats, pairing one of the three pigments with a short-wave pigment
common to all individuals, whereas females may be either dichromatic or
trichromatic. At present we have good evidence for only one form of
trichromacy, the P564 combined with the P543 Travis et al., 1988) but
with indications (unpublished) of the other two predicted variants. In its
simplest form the genetic model suggests that two-thirds of females are
trichromatic. However, within our limited sample of marmosets, there
appear to be fewer trichromats than the model predicts.
.
Spectral Location of Pigments
Within the primates both from the Old World and the New World,
there would appear to be distinct spectral locations for cone photopigments
in the red-green spectral range. Thus, Old World monkeys (including
humans) have pigments at 535 and 565 nm, while New World monkeys may
have one of these but may also have intermediate pigments with Oman at
about 543, 550, and 557 nm. This is illustrated in Figure 3, which shows
the pigments found in each species, and there are indications of specific
spectral locations each separated by about 6 to 7 nm. The same spacing can
be applied within mammals generally (see Jacobs, 1987) and is reminiscent
of the idea of "clustering" of visual pigments first proposed by Dartnall
and Lythgoe (1%5) for extracts of rod visual pigments (see also Knowles
and Dartnall, 1977, pp. 195-199~. Presumably there are constraints on the
structure of opsins such that variations in their amino acid sequences do
not result in visual pigments with a continuum of spectral sensitivities but
in pigments that lie at discrete spectral locations.
Can such a hypothesis reveal anything about the spectral location of
anomalous pigments in colour-deficient human observers? The work of
Nathans et al. (1986) has shown that the opsin sequences of the long-
and middle-wave cone pigments in humans are more than 90 percent
homologous and that in anomalous trichromats the hybrid genes probably
OCR for page 26
26
0
._
~ 4
Q
o 2
JAMES K BOWMAKER
430 530 550 570
Waveleng th nm
FIGURE 3 Distnbution of values of the mean peak sensitivities of the cone types identified
in humans, four species of Old World Inmates, and two species of New World primates.
Note the dominant peak wavelengths at about 565, 535, and 430 nm and the suggestion of
clustering with a wavelength interval of about 5 to 8 nm.
encode for the pigments that lie between the normal long- and middle-
wave pigments. The clustering of primate pigments implies that there are
potentially three spectral locations for these pigments—543, 550, and 557
nm. It is interesting that in analyses of psychophysical measurements on
anomalous observers, Pokorny et al. (1973) estimated that the normal and
anomalous pigments are separated by only 6 to 7 nm. Thus, protanomalous
observers may have a P535-P542 combination, whereas deuteranomalous
observers may have a P564 combined with a P557. Unfortunately, no direct
measurements of anomalous pigments by either microspectrophotometry or
suction electrode techniques have been made. The only such measurements
from the eye of a color-deficient observer are those from a deuteranope,
where only short- and long-wave cones were identified (Mollon et al.,
1984a).
SHORT-WAVE CONES
Old World Monkeys and Humans
Attempts to establish by microspectrophotometry the spectral location
and shape of the absorbance spectra of short-wave cone pigments have been
made more difficult by the relative rarity of short-wave cones, normally less
than 10 percent of the cone population, and by the problems of short-
wave scatter and the probable contamination of spectra by photoproducts
(for a discussion, see Mansfield et al., 1984~. The best estimate for the
Oman of short-wave cones in macaques would appear to be about 430 nm
OCR for page 27
CONE VISUAL PIGME~S IN MON=YS ED HUMS
27
(MacNichol et al., 1983; Mansfield et al., 1984~; our more recent data from
four species of plattyrhines support this value (Table 1~.
In the moustached guenon we obtained data from six short-wave cones;
the mean absorbance spectrum is shown in Figure 4a. These prebleach
spectra may be contaminated by short-wave light scatter and by photostable
pigments. Each cone was exposed to white light to bleach the photopigment,
and the spectrum was measured again, from which a difference spectrum
representing the bleached photopigment could be derived (Figure 4a). The
difference spectrum should eliminate problems caused by light scatter and
photostable pigments, but it may be distorted by photoproducts. The AmaX
of the prebleach and that of the difference spectra were then determined by
fitting the template curve to the right-hand limb. As can be seen, both sets
of data are best fitted by a template with Oman; at about 431 nm. Similar
fits were obtained for the rhesus, talapoin, and baboons, and the overall
Oman was again 431 nm. This value is identical to that reported by Baylor
et al. (1987) from suction electrode measurements of spectral sensitivity in
short-wave cones from macaques.
In humans the situation appears to be different. In Figure 4b the mean
spectra from four human short-wave cones are shown, with a template
curve with )\maX 420 nm superimposed. Although the difference spectrum
Is narrower than the template, it is clear that the spectra lie at wavelengths
distinctly shorter than those of Old World monkeys. The Oman of 420
nm agrees with our earlier published data for human short-wave cones
(Dartnall et al., 1983~.
New World Monkeys
In the rebid, Saimir' sciureus, we have data from 16 short-wave cones.
The spectra, both prebleach and difference, are best fitted by a template
curve with Oman at about 430 rim (for spectra, see Mollon et al., 1984b;
Bowmaker et al., 1985~. The photopigment is clearly spectrally very similar
to those in Old World monkeys. However, the short-wave cones in the
callitrichid, Callithr~x jacchus, appear to be different. The mean spectra
from 14 cones are shown in Figure 4c and are best fitted by a template
with Ama2; at about 424 nm (Travis et al., 1988~.
Spectral Location of Pigments
As with the photopigments maximally sensitive in the red-green spectral
region, the short-wave pigments of primates also appear to cluster at distinct
spectral locations those of Old World monkeys and squirrel monkeys
cluster at about 431 nm, that of the marmoset at about 424 nm, and that
of humans at about 420 nm (Figure 3~. The mean spectra for the three
pigments are shown together in Figure 4d, where the spectral displacements
OCR for page 28
28
JAMES K BOWMAKER
100
O L
O
I ~ I I r I I I r I ~ I r I I I r I I I lil I ~ I ~ ~ ! I
, \
_~
4)
c
o
53
o 100 _ ,f\~;
~ ,. '.
~ ~ a~ ~
. .~
-
I ~ ~ ~ I ~ 1 l 1 i ~, ,,r I I' 'Tl 111 1 I r 1-11
_f
_
_
!, 1 . , 1,, I 1 1 t' 1 1 ,, 1 . , 1 , 1 ~,,
-
| ! I I ~ | I ~ I I i I ~ ~ I I I I ~ ~ I I I I I I I ~ I I i ~ I ~ ~ I ~ I ~ I I ~ ~ I ~ I ' I ~ ~ I I I I ~ ~ ~ I I I
450 550 650 450 550 650
r I I T-r I I I 1 1 1 i I I 1 ~ 1 1 1 1 1 I I I I I I r r ~ I I r I I r I ~ I I ! I r I j I I I ! ! I
1nn ~ c ~ d -
- ~ 1 [, 1 1 1 1,,,, ! i,, .~ ~, ~ ~ '
450 550 650 450 550 650
Wavelength nm Wavelength nm
FIGURE 4 Absorbance and difference spectra from short-wave cones of primates. The
top panel of each pair plots the mean absorbance spectra before and after bleaching, and
the bottom panel plots the difference spectrum derived from the bleaching. The prebleach
spectra and difference spectra have been normalized to 100 percent. In the upper left are
the mean spectra from SL~ cones from Cercopithecus cephus (moustached guenon), with a
431-nm template superimposed. In the upper right are the mean spectra from four cones
from human eyes, with a 420-nm template. In the lower left are the mean spectra from
14 cones from Callahr~r jacchus (common marmoset), with a 424-nm template. In the
lower right is a comparison of the mean spectra from Old World primates (longest-wave),
Callithnx (middle-wave), and humans (shortest-wave).
OCR for page 29
CONE VISUAL PIGMENTS IN MONKEYS AND HUMANS
29
are clear. Again, this is reminiscent of the Am spacing of the longer-
wave pigments (Figure 3) and may imply that there are constraints on
the structure of visual pigments that determine their spectral sensitivities.
Clearly, to elucidate such problems, more information is needed on the
amino acid sequences of a number of primate opsins as well as a further
understanding of the tertiary arrangement of opsin and retinal within the
disc membranes of the cone outer segments.
ACKNOWLEDGMENT
lithe microspectrophotomet~y summarized here was conducted with
support by the Medical Research Council of the United Kingdom grant
G8512759N.
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Representative terms from entire chapter:
world monkeys
