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OCR for page 2
Optical and Molecular Design of Rods
WILLIAM H. MILLER
INTRODUCTION
Thank you, Bob Shapley, for such a kind introduction. I greatly
appreciate it.
In trying to strike a keynote both melodious and strong enough to
resonate with this audience, I think of Franz Boll, who proposed the
photochemical theory of vision. Although he died of tuberculosis at the age
of 30, before he had an opportunity to exploit his great discovery of visual
purple, there is no doubt that he appreciated its potential as discussed in
Hubbard's (1977) preface to her translation of his paper.
Not only did Boll propose the photochemical theory of phototrans-
duction, but he also proposed a photophysical theory, which has found
application in explaining the color of another of his discoveries, the green
rod. Because I have been interested in transduction and the green rod, I
want to share some of my thoughts on both of these problems with you.
GREEN ROD
Boll's green rod represents a design problem dealing with both visual
pigments and image sampling. Neither the rod's color nor its role in sam-
pling is completely understood. Alla n Snyder and I have proposed that the
green rod myoid is a wavelength filter (Miller and Snyder, 1972~. Reuter
and Virtanen (1972) showed that the green rod is the short-wavelength
receptor for a color opponent process at photopic and mesopic light inten-
sities. In contrast to the thin rods with pooled responses of many species,
Jagger (1988) suggested that amphibian fat rods may individually sample
2
OCR for page 3
OPTICAL AND MOLECULAR DESIGN OF RODS
3
FIGURE 1 End-on appearance of pink and green rods. Pink rods are bleached; green
rods retain their green color SOURCE: Boll (1877~.
the eye's image. The green rod may function with both the rod and cone
systems for image sampling and color vision.
Green Color Not Caused by Visual Pigment Alone
Boll was the first to describe the green rod. He proposed a photo-
physical theory of vision in addition to his photochemical theory because
he was uncertain as to the origins of rod colors (Boll, 1877~:
As against this photochemical theory of the nature of visual red and of the
light sense, another formulation is possible which in contrast might be called the
photophysical theory. This theory assumes that there is no special pigment that
permeates the rod stroma, but attributes the red color of the rods to a purely
physical phenomenon, the optical effect of stacking of intrinsically colorless
platelets. Accordingly visual red would belong to the category of interference
phenomena and more specifically to the narrower class of the so-called colon
of thin films.
The photophysical theory of vision was not taken seriously after
Kuhne's characterizations of rhodopsin. Nevertheless, this concept was
plausible at the time. The dimensions of the rod platelets would not be
known for 75 years, and in fact such platelets are found to produce inter-
ference colors in the optical trains of both invertebrate and vertebrate eyes.
More to the point, a photophysical theory has merit when applied to the
case of the amphibian green rod.
Figure 1 is a black and white reproduction of part of Boll's 1877
color plate showing the frog rod mosaic with its pink and green rods after
illumination with short-wavelength light. The dark spots are green in the
original color plate, and the light spots representing the bleached pink rods
are colorless.
Figure 2 is a scanning electron micrograph of part of the photoreceptor
layer of a preparation of an amphibian retina similar to that used by Boll.
Although the green rod has a shorter outer segment than the pink rod, it
nevertheless retains its green color after the pigment of the pink rod has
OCR for page 4
WILLL4M H. MILLER
FIGURE 2 Scanning electron micrograph of amphibian photoreceptor layer showing a
few single cones, many pink rods, and one green rod with its 1-micron diameter myoid.
NOTE: Arrow indicates the external limiting membrane
been bleached, as shown in Boll's figure. This was confirmed by Liebman
and Entine (1968~:
It is of some interest that our green rods show no light absorption in the red-
orange region that would explain results of Denton and Willie who found such
absorption in end-on measurements using photographic densitometty (Demon
and Wyllie, 1955~. Nor, after bleaching, was an increased absorption found in
the green region of the spectrum....We can therefore state categorically that
the locus of the green and red absorbing entities is not in pigment form in rod
outer segments.
Similarly, a year earlier Dartnall (1967) also reached the conclusion that
the yellow-red absorption may "even possibly be a structural color."
OCR for page 5
OPIICAL AND MOLECULAR DESIGN OF RODS
s
Myoids Are Waveguides
Miller and Snyder (1972) proposed that the myoid's waveguide prop-
erties in combination with the rod's 433-nm pigment could account for the
green color. The assumption underlying this hypothesis is that the parts
of the photoreceptor cells that are located sclerad to the external limiting
membrane (horizontal arrow, Fig. 2) are light pipes. The green rod's aper-
ture is its myoid near the external limiting membrane. Light that reaches
the outer segment must first pass through the myoid. The physical prop-
erties of the myoid, its diameter and the difference between its refractive
index and that of its surround, should determine the intensity and spectral
distribution of the light that reaches the green-rod visual pigment.
The green rod's unbleached end-on color in white light results from
absorption in the blue by its 433-nm pigment and "absorption" of yellow
and red by an unknown structure. The myoid could be that unknown
structure. Yellow-red light would be lost not by absorption but by not
being propagated in the waveguide by total internal reflection. The light
propagated in waveguides shows intensity patterns called modes, when the
guide is viewed in cross section. For each mode the fraction of modal
energy propagated inside the guide is a monotonic function of the ratio of
guide diameter (d) to wavelength (~) and of the difference in refractive
index between the guide (ins ~ and its cladding (nay. The smaller d is relative
to ~ and the smaller no—n2, the less longer-wavelength light will reach the
outer segment. The fraction of light energy inside the guide, '7, is equal to
1 - (7rdul) (o2 02) (TIC)
where be, the complement of the critical angle, is equal to 1 - (n2/n~2
and ~ is the angle of incidence, which is a function of the mode number
(equation from Snyder, 1975:p.44~.
The fraction of light (~) that would be inside a myoid of 2 Em (Figure
3 curve c), 1 Em (curve a), 0.8 Em (curve b) and 0.5 Em diameter (curve
d) is plotted as a function of wavelength based on the two lowest order
modes in Figure 3 from Miller and Snyder (1972~.
Curve a of Figure 3 shows that the dark-adapted myoid with a diameter
of 1 Em diameter would propagate yellow-red wavelengths poorly in com-
parison with shorter wavelengths. When viewed end on, the combination
of decreased propagation in the yellow-red and absorption in the blue by
the 432 rim pigment could cause the green appearance of the dark-adapted
green rod. According to Arey (1916), the green rod myoid becomes slightly
more tenuous when light-adapted. A 0.8 Em diameter would shift the curve
to the left as shown by curve b, to mimic what was interpreted by Denton
and Wyllie (1955) as an increased green absorption in the light-adapted
OCR for page 6
6
WILLIAM H. MILLER
10
. _
~^ 0 8
. _
3 06
-
° 0-4
o
0 02
. _
t
~ o 1
2'Lm
~ 05f~m
,Lm
fib
1
1
300 350 400 450
500
Green
550 600 650
U ~
Yellow Red
FIGURE 3 Theoretical effect of myoid diameter on fraction of light inside the myoid as
a function of wavelength for the two lowest-order modes. SOURCE: Miller and Snyder
(1972).
end-on preparation. An even smaller diameter myoid, as illustrated in
curse d, would tend to cut off much of the light in the visible spectrum.
Green Rod Function
Green Rods May be Color Receptors
If we accept that the green myoid in combination with the outer-
segment 433-nm pigment can explain the rod's end-on color, that still
leaves the problem of its function. Reuter and Virtanen (1972) have said:
Our experiments suggest the existence in the frog retina of separate channels
for green rod responses. When during dark adaptation the red rods begin to
contribute they enter the on-off and off channels of the class 1, 2 and 4 cells, that
is the cone but not the green rod channels. This makes possible color vision in the
mesopic state. The red rods simply contribute to the cone side of the opponent
color system. This arrangement, together with the fact that the cone channels
dominate and are sufficient for eliciting all the Maturanna et al. characteristics,
guarantees the invariance of coding of brightness pattern information during the
shift from photopic to scotopic vision.
The main role of the green rod channels seems to be to "add color to the
system."
OCR for page 7
OPIICAL AND MOLECULAR DESIGN OF RODS
TABLE 1 Amphibian Rod and Cone Parameters
7
Green Rod Pink Rod Single Cone
Outer-segment diameters)
Dark-adapted entrance
aperture (myoid at external
limiting memberane)
4,um Plum 2.5~n
=0.8pm2 ~28pm2
Outer-segment optical
density, peak absorbance(a) 0.68 0.82 0.26
Relative anatomical
sensiiiviy (absorbance x
capture area)
Sensitivity at peak
wavelength (mV/quantum)(b~)
Nyquist frequency based
on posterior nodal
distance = 5 mm (c/deg)(d) 2
0.6 23
~10 =10
7
~S[lm2 Qight adapted)
1
1
?
(a)Lieb~nan and Entine (1968) (Rana)
(b)Fain and Dowling (1973) based on intracellular recordings in intact retina, which may
exaggerate sensitivity of rods because of coupling.
(C7Reuter and Virtanen (1972) sensitivity at peak wavelength measured at ganglion cell.
(Jagger (1988) (Bunko). Green rods comprise 11% of total in plate la, ref.2; Nyquist
frequency calculated assuming pink rod number density = 18000/mm2 and green rod number
density = 1800/mm2.
Are Individual Fat Rods Samplers?
The rods may provide spatial vision matched to the optics under
mesopic conditions, according to Jagger (1988~. Jagger argues that the rods
could effectively sample the 6 cycles per degree image quality found over
most of the eye's visual field. Some amphibian rod and cone parameters
drawn from various sources are shown in Table 1.
The green rod appears to be more sensitive than the single cone
and may function as a color receptor. Comparison of the image sampling
properties based on the information in the Table 1 is difficult because
of the wide range of eye sizes among amphibian species. Using a 5-mm
posterior nodal distance (PND) eye as a sample eye size, the green rods by
themselves would not be useful for spatial resolution because they could
support only a Nyquist frequency of 2 cycles per degree. It seems likely,
therefore, that the green and pink rods function as a unit for color and
spatial vision based on a flat 6 cycles per degree optical quality over most of
the retina. There would be some undersampling (Snyder et al., 1986) by the
ganglion cells in the region of peak density where the potential maximum
acuity would be 4.4 cycles per degree, and there would be less than 3 rods
per ganglion cell away from the visual streak. Nevertheless, the theory that
OCR for page 8
8
WILLIAM H. MILLER
the fat amphibian rods individually sample the retinal image is plausible,
considering that there is much image processing prior to the ganglion cells
in the amphibian retina and there is an early optokinetic acuity measure of
4.4 cycles per degree for Rana (reviewed in Jagger, 1988~.
Rods and cones might be expected to have small diameters not only
because separate optical channels should be as small as possible, consistent
with the diffraction limited image, to maximize resolution but also to
facilitate temporal resolution by limiting diffusion transit times. Rod outer
segments of many animals ranging from fish to mammals are about 2
Em in diameter. Those of amphibians are 6 Em or larger. A design by
which amphibian fat rods may provide the same effective resolution over
the entire visual field in amphibians contrasts with that of many retinas
with thin rods in which the rod responses are pooled to provide increased
sensitivity at the expense of resolution. The green rods may have evolved
to contribute to both color and form vision.
TRANSDUCTION
For the study of transduction that Boll initiated, it is now generally
accepted that the rising phase of the vertebrate photoreceptor response is
mediated by activation of phosphodiesterase (PDE) and that recovery is
mediated at least in part by activation of guanylate cyclase (cyclase). But
there is controversy regarding whether inhibition of PDE contributes to the
initial phase of recovery. Hiroaki Kondo and I (Kondo and Miller, 1988)
suggested that the initial phase of recovery is driven by increased rather
than decreased PDE activity. Increased PDE activity may lead to decreased
[Caii and activation of cyclase to both truncate the response and cause the
smaller amplitude and faster recovering light-adapted response.
Photolyzed rhodopsin activates a cyclic nucleotide enzymatic cascade.
The concentration of cyclic GMP is reduced causing decreased plasma-
membrane conductance (Fesenko et al., 1985) and the decrease in dark
current that is the response to illumination (see Pugh, in this volume; Stryer,
1986~. Details of the recovery process and light-adapted response are still
not well understood. That calcium plays a role is generally accepted:
cytoplasmic calcium concentration (jCaii) falls during the light response
and that fall in [Caii is thought to either inhibit phosphodiesterase activity,
activate guanylate cyclase activity, or both, to restore the concentration of
cyclic GMP.
Is Response Recovery Mediated Initially by Cyclase Activation?
The development of the concept that recovery is mediated by activation
of cyclase rests on the synthesis of two experimental facts: the finding of
OCR for page 9
OPTICAL AND MOLECULAR DESIGN OF RODS
9
McNaughton et al. (1986) that [Call is decreased by illumination and the
findings of Lolley and Racz (1982), Pepe et al (1986) and Koch and Stryer
(1988) that very low [Ca~i activates cyclase. Hodgkin et al. (1985) combined
the first hints of these findings with their observation that calcium does not
close channels as rapidly as light:
Another possible explanation of the failure of calcium ions to close channels
rapidly is that calcium might inhibit the production of a substance which keeps
channels open rather than interacting directly with the channels.
What could that substance be? On one hand, Cyclic GMP is a candidate
based on evidence that that substance increases conductance of an excised
patch of ROS plasma membrane (Fesenko et al. 1985~. On the other
hand, though cyclic GMP increases channel conductance, whether that is
because it binds the channel directly is not known, since the patch contains
substances other than the ROS plasma membrane (Kolesnikov et al., 1987~.
Nevertheless, measurements of [Ca~i have been continually refined.
Dim illumination takes the dark resting level from 220 nM to ~140 nM
(Ratto et al., 1988~; strong illumination has been calculated to give a
minimum value of 60 nM (Miller and Korenbrot, 1987~. At the same time
the evidence that cyclase is activated by nM levels of calcium has become
convincing. Lolley and Racz (1982) were the first to use calcium at nM
concentrations. Pepe et al. (1986) were able to duplicate Lolley and Racz's
result on rat rods in dim red light, but only when their homogenized toad
rods were illuminated. On the other hand, Koch and Stryer (1988) found
that the activity of unilluminated bovine ROS cyclase was regulated by a
highly cooperative calcium-dependent molecular switch (not calmodulin).
Guanylate cyclase was activated up to 20-fold when [Ca] was reduced from
200 to 50 nM from a basal rate of 7 ~uM cyclic GMP/sec/ROS to 100 EM
cyclic GMP/sec/ROS. Since [Caii may decrease from about 200 to 60 EM as
a result of illumination, Koch and Stryer's evidence leads to the suggestion
that the free concentration of cyclic GMP decreases only transiently in
response to a flash, because low Ca rapidly triggers restoration of cyclic
GMP levels. Pugh (in this volume) recounts other in press evidence to the
same effect.
Disagreement Regarding Role of PDE Inactivation
While there is agreement that low [Caii aids recovery by activating
cyclase, there is still no agreement as to whether the low [Ca]' also inhibits
PDE. There is conflicting biochemical evidence regarding the rate of PDE
inactivation. Recovery of PDE to its basal level is controlled by the rate
of hydrolysis of GTP bound to alpha-transducin, Ta. On the one hand,
the rate constant for transducin's GAP hydrolysis was measured to be 0.02
see-i (Bennett and Dupont, 1985), while other measurements show a
OCR for page 10
10
WILLIAM H. MILLER
half life for Ta-GTP of 3 sec at 23° for cattle rods (Vuong and Chabre,
1988~. Decreased PDE activity would of course aid recovery of cyclic GMP
levels near the plasma-membrane channel. In this vein, Pierre et al. (1986)
conclude:
The results are consistent with the idea that the rapid drop in Cai, which has
recently been shown to accompany the light response, is involved in terminating
the light response, and that Cai is thereby involved in setting the operating point
and sensitivity of phototransduction. From the comparison with other work we
infer that Cai appears to act, at least in part, by means of control of cGMP
phosphodiesterase activity.... Hence we conclude that elevated Cai leads to
enhanced activity of PDEase.
An alternative hypothesis holds that lowered [Caii is involved in ini-
tially terminating the light response not by inactivating PDE as suggested
by Torre et al. but rather by activating cyclase.
Light Response Recovery Because of PDE Activation?
Uniform pC cyclic GMP injections into ROS at the resting potential
cause cyclic GMP depolarizing responses of uniform amplitude and du-
ration, as if the cyclic GMP responses provide an index of PDE activity.
Corresponding with PDE activation by light, cyclic GMP responses are
antagonized in a graded manner with increasing intensities of illumination
(Miller, 1982~.
Uniform 5 pC cyclic GMP pulses were delivered before during and
after a 0.1 sec bright light flash in the experiment shown in Figure 4A.
The cyclic GMP pulses are numbered 1-10. Each downward spike was an
injection artifact. The numbered upward depolarizations were the cyclic
GMP responses. The increased PDE activity that mediates the receptor
potential was sufficient to reduce the amplitude and speed the recovery
of cyclic GMP response number 2 in comparison with that of number
1. Although the receptor potential recovered rapidly, PDE activity (as
reflected in the amplitude and recovery rate of the cyclic GMP response)
continued to increase and did not recover to the preflash levels until
more than a minute after the receptor potential recovered. The receptor
potential recovered rapidly despite apparently high PDE activity. The light
flash intensity was reduced by half and the flash duration was lengthened in
Figure 4B. The recovery rate of the cyclic GMP responses was more nearly
matched to that of the receptor potential. Finally in Figure 4C, in which
the light flash was a log unit dimmer than that of Figure 4B, the recovery
rate of the receptor potential matches the recovery rate of the cyclic GMP
response (and presumably PDE activity).
The initial very rapid recover from a bright flash occurs despite an
apparent high rate of PDE activity, which implies that the concentration
of cyclic GMP must be restored by cyclase activation rather than PDE
OCR for page 11
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Representative terms from entire chapter:
green rod
OPTICAL AND MOLECULAR DESIGN OF RODS
1
8 9 10
A it.
,-4 1c~ uni as
1 ~ 1 1 1 - ~ 1 Pi 1
B
.
|10mV
10s
ffl
12
pA
WILLIAM H. MILLER
~ .
c o r1 t ~ o 1 \ ~ ~
~~ it=
3
FIGURE 5 Suction current responses to light flash before and after application of
p[NH]ppG to rod outer segment by whole-cell patch. Response after ptNH]ppG is scaled
up by factor of 2.17 for normalization. Response after p[NH]ppG is truncated presumably
by cyclase activation as indicated in Figure 6.
explained by a model in which the initial stage of recovery is mediated by
an increase rather than a decrease in PDE activity.
We obtained additional support for this hypothesis by testing whether
the response to a light flash can recover when PDE activated by the flash
is inhibited from deactivation by the introduction of the nonhydrolyzable
analog of GTP, guanyl-5'-yl imidodiphosphate, p[NH]ppG, into the outer
segment using the whole-cell patch clamp technique (Kondo and Miller,
1988~. The p[NH]ppG both reduces the amplitude of the response and
hastens the initial segment of recovery (Figure 5~.
A previous experiment in which a hydrolysis resistant analog of GTP
was patched into the outer segment gave a different result. There was no
response recovery when 500 ,uM GTP-^y-S was applied to the isolated outer
segment (Sather and Detwiler, 1987~. The difference between these two
results is difficult to explain in the absence of information about the Km's
of the various analogs and of GTP for cyclase, but a preliminary report
of 1-2 mM ptNHippG patched into the inner segment of the isolated rod
(Lamb and Mathews, 1986) appears to show results similar to those of the
whole cell rather than the isolated outer segment.
The effects of piNH]ppG may be explained by a model in which
activated transducin leads to a new steady state of lowered dark current
and hence sensitivity. An added test flash rapidly leads to still lower
cytoplasmic calcium concentration, and because of the steepness of the
calcium dependence of cyclase, the concentration of cytoplasmic cyclic
GMP is driven rapidly higher to truncate the response. The later and slower
component of recovery would be mediated by Ta.GTPase. This analogy
between the effects of ptNH]ppG and the effects of light adaptation leads
to the suggestion (Kondo and Miller, 1988) that transducin activated by
photolyzed rhodopsin is the signal that controls the initial rod response
recovery following a bright flash as well as the rapid initial recovery and
OPTICAL AND MOLECULAR DESIGN OF RODS
g-cyclase.
to
[Ca i] ~
ROS inward
Ca current
GTP ~
~ 5'GMP - ~—
-
~ PDE*
13
/
cyclic GMP
T*`
R*
FIGURE 6 Schematic of hypothesized molecular mechanism of initial response recovery
and of light adaptation of rod photoreceptor. Light revs up PDE~dase cycle, causing it to
race. Light adaptation reduces the ROS inward calcium current and [Caii, which activates
g-pyclase to rapidly increase cyclic GMP levels, which truncates response.
reduced sensitivity of the light-adapted response by means of acceleration
of the PDE-cyclase cycle as indicated in Figure 6.
CONCLUSION
Remarquez bien que les nez ont ete fan's pour porter des lunettes, aussi
nous-avons des lunettes.
Candide, Ch. 1:38-39
The speculators continue to give rise to suggestions for optical and
physiological photoreceptor functions following the good example of Franz
Boll, who was the first to practice this art in visual science. The suggestions
presented at this symposium are grist for the mill. Because observation
14
WILLIAM H. MILLER
continually improves, these speculations on the path to knowledge can
never be accepted as final. Getting there is all the fun.
ACKNOWLEDGMENTS
This work was supported mainly by National Institutes of Health grant
EY03196 and in part by NIH Vision Center grant EY00785, Research to
Prevent Blindness, Inc., and the Connecticut Lions Eye Research Founda-
tion.
Note added in proof: There have been significant developments since
this manuscript was written. 1. Additional evidence that calcium may
mediate the light-adapted response was published; reviewed by: E. Pugh
and J. Altman (1988) A role for calcium in adaptation. Nature 334: 1~
17. 2. Studies showing cyclic GMP Sated channel activity lent additional
support for the theory that cyclic GMP may mediate transduction by directly
binding the light-sensitive channel: J.W. Clack and P.J. Stein (1988) Opsin
exhibits cGMP-activated single-channel activity. Proc. Natl. Acad. Sci
USA 85:9806 9810 and U.B. Kaupp, T. Niidome, T. Knave, S. Ibrada, W.
Bonigk, W. Stuhmer, N.J. Cook, K Kangawa, H. Matsuo, T. Hirose, T.
Miyata, and S. Numa (1989) Primary structure and functional expression
from complementary DNA of the rod photoreceptor cyclic GMP-gated
channel. Nature 343:762-766.
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1985 The G-protein of retinal rod outer segments (Transducin). The Journal of
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OPTICAL AND MOLECULAR DESIGN OF RODS
15
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16
W7LLLAM [I. MILLER
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