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The Tohoka Journal of Experimental Medicine, Vol. 58, No. 1, 1953
Two Kinds of Scotopic Mechanisms in
the Human Retina
By
Toshihiko Oikawa
From the PhysiologicalLaboratory of Prof. K. Motokawa
, Tohoku University,Sendai
(Received for publication, September 9, 1952)
INTRODUCTION
In the duplicity theory it is assumed that scotopic and photopic
vision are mediated by rods and cones respectively. Although the evi
dences have steadily accumulated in favor of the idea of two separate
modes of vision,-14) it is possible that the cones can, in certain cases,
function to some extent in night vision, retaining some of the attributes
of the more primitive mechanism from which they are evolved.15-16)
The elaborate work by Polyak17)has directed our attention to the
fact that besides the photoreceptor cells, there is a host of other structures,
far too numerous and peculiarly organized to be ignored in the retina.
We have now strong evidences that the cones and the rods converge into
a final common path.17-18) If the cones and the rods function so separate-
ly as the duplicity theory assumes, the interconnections in the " intermedi
ate zone "19-70)are difficult to understand.
Motokawa and his associates21-23)have provided a means by which
the photopic and the scotopic process can clearly be separated from each
other. It is probable that the processes revealed by this method represent
physiological events in the intermediate zone rather than at the receptor
or the cortical level.20)24-25)
It has been believed that the cones have nothing to do with achromatic
twilight vision 4)26-21)but the present investigation has revealed that in
the intermediate zone there occurs another kind of scotopic process having
some characteristics of cone-processes, besides the so-called rod-process
below the color-threshold. It is the object of the present paper to identify
this newly discovered scotopic process and to elucidate its physiological
significance.
70 T. Oikawa
EXPERIMENTAL
Method
The method consisted in measuring the electrical sensitivity of the eye after exposure to a brief illumination. A preliminary dark adaptation of about 40 minutes was allowed before making any electrical and photic stimulation. The electrical stimulus used was a single constant current pulse of 100 msec. in duration. The current was applied through a pair of silver electrodes placed slightly above the eyebrow and on the homo- lateral temple. Thus, the threshold voltage was determined to produce the least perceptible electrical phosphene. The effect of an illumination was expressed as a percentage increase of the electrical excitability over the resting level and denoted by ƒÄ. Retinal areas 20ƒÍ and 50ƒÍ from the center of the fovea were exposed to a circular patch of 2? in visual angle illuminated by spectral light, and at different times after removal of the light stimulus the electrical excitabili ty was determined to construct a ƒÄ-time curve. The duration of pre illumination was made 0.5 seconds for the reasons stated in a preceding paper.23) For further details of experimental procedures previous papers24)29) should be consulted. The intensities of spectral lights used for pre-illumination ranged between the light- and color-threshold. Thresholds for photic stimuli were determined by the method of limits: The light was diminished in intensity until it was not seen, and, in alternating runs, was increased until it was seen. The average of ten such measurements was taken as the threshold value. In such measurements the duration of a single flash was made 0.5 seconds. The color sensation felt by the subject at the color-threshold was either yellow or blue according to the wave-lengths of spectral lights. It was found difficult to perceive any definite coloration near 505 mp. Accuracy of measurements Fluctuation in the excitablity of the resting eye can be a -cause of errors. Daily variations of the resting threshold voltage in our experi ments were found to lie between 0.8 and 1.6 volts. The resting threshold had to be measured almost each time, and when it was found different more than 10% before and after a measurement, the latter was discarded. When fluctuations became too remarkable for some reasons, for example, due to fatigue, measurements were stopped at once. We used to determine from 5 to 10 points in a session, and a series of experiments was completed in a few sessions. The reproducibility of C-values was, however, so satis factory in well-trained subjects that points determined in different sessions yielded a smooth curve.
72 T. Oikawa
Fig. 1. Ā-time curves obtained at 20? from fovea at three intensity levels; i.e. light-, color- and proper color- threshold. Ordinates: percentage increases of electrical excitability of the human eye above resting level (Ā). Abscissas: time in sec. after termination of pre-illuminating light. The duration of pre- illumination was 0.5 sec. except for dotted curve.
appear in the curves obtained at the light-threshold. This was indeed beyond our expectation that only rod-processes would appear under this experimental condition. In the curve for green light we encountered double thresholds when stimulating voltages were graded in sufficiently small steps. This was due to overlapping of the two processes, the rod-process on one hand, Y or B on the other. The same is the case with the curve for yellow light. In order to make certain that the double thresholds were really caused by such over- lapping, measurements were carried out under the experimental conditions under which no rod-process appeared: According to Motokawa et al.21-22) no rod-process manifests itself when the pre-illumination is longer than 4 seconds. The dotted curve was obtained, using yellow light of 4 seconds and of intensity just corresponding to the light-threshold for pre-illumi nation. The curve shows distinct maxima at 1.5 and 3 seconds, but the rod-process can be seen no more. According to the analysis by Motokawa24), the Ā-time curves for red,
yellow, green and blue receptors show a maximum at 1, 1.5, 2 and 3 seconds respectively. If the result of Motokawa's analysis is applicable to the data obtained with such low intensities of pre-illumination in our experiments, then it may be said that the maxima at 1.5 and 3 seconds
Two Kinds of Scotopic Mechanisms 73
in our curves are to be ascribed to the yellow and the blue receptor re
spectively. -Hence they are denoted by Y and B. Another aspect: to
be mentioned is that the magnitudes of the Y and B processes are nearly
equal to each other in all curves.
Quite similar curves to those illustrated above were-obtained at 50o
from the foveal center. The intensity of pre-illumination was slightly
above the light-threshold, the other experimental conditions being the
same as above. They are illustrated in Fig. 2. In the set of curves the
three elevations are found more conspicuous than in the curves at 20o
illustrated in Fig. 1. Such clearer separation of the three processes at
50o has been caused by the circumstance that the rod-process is lower at
50o than at 20o. This finding fits in with the known properties of rods
that their population density is smaller at 50o than at 20o.30) On the
other hand, the magnitudes of the Y and B processes at 50o are almost
the same as at 20o. This finding may correspond to the known fact that
the population density of cones at 50o is nearly the same as at 20o.
Fig. 2. Ā-time curves at 50o from fovea; other notations the same as in Fig. 1.
T he curves show that the magnitudes of the three processes, Y, B
and ROD depend little on the wave-lengths of spectral lights. This
relation can be seen more clearly in Fig. 3A, in which the magnitudes
Two Kinds of Scdtopic Mechanisms 75
Another series of experiments was carried out at the color-threshold. The results are shown in the middle column of Fig (^). 1. The C-time curves
generally consist of two elevations which can be identified with the Y- and the rod-process for red, yellow and green lights and with the B- and the rod-process for blue light. It is to be noted that either of the two components of the twin-process is depressed at the color-threshold. This relation is seen more clearly in the spectral distributions of the Y-, B- and rod-processes determined at the color-threshold in Fig. 3B. As can be seen in this figure either component Y or B of the twin-process is depressed according to whether the wave-length of pre-illuminating light is shorter or longer than 505 mƒÊ. This finding just corresponds to the psychological fact that at the color-threshold of the peripheral retina, spectral lights of longer wave-lengths give rise to a yellow sensation, while those of shorter wave-lengths elicit a blue sensation .31-33) At 505 mp it was found difficult to determine the color-threshold because of a high degree of desaturation. The rod-response showed a flat rise in the mid-spectrum similar to that observed at the light-threshold. Next, the dependence of the magnitudes of the twin-process and rod- process on the intensity of pre-illuminating light was investigated. In Fig. 4 the magnitudes are plotted as ordinates against the logarithms of the intensities in physiological units as abscissas. Between the light- and color-threshold these magnitudes remain constant irrespective of the in- tensity. Above the color-threshold the Y and the rod-process increase as the intensity of red light rises, whereas the B component of the twin- process is out of sight (A), and the Y component is in turn depressed in the case of blue pre-illuminating light (B). It seems that the all-or-none law approximately holds for the depression of the Y or B component of the twin-process. It is to be noted that the depression of either component of the twin- process is the only change that occurs with the development of a color sensation, blue or yellow. As can be seen in Fig. 4, the Y and B components of the twin-process are equal in magnitude in the colorless interval and are complementary to each other. Therefore it is probable that the twin-process subserves colorless sensations as does the rod-process. They must co-operate with each other in producing colorless sensations below the color-threshold. Thus the present experiment has provided evidence that there are two kinds of scotopic mechanisms in the human retina. In the right column of Fig. 1 two ƒÄ-time curves are illustrated, which were obtained for red and green lights of intensities high enough to elicit specific color sensations of red and green (the proper color-thrshold).
76 T: Oikawa
Fig. 4. Relation between magnitudes of Y-, B- and rod-processes and logarithm
of light intensity. Procedure of experimentation is shown in inset.
The crest time of the preceding elevation of the curve for red light is now 1 second instead of 1.5 seconds, while that of the preceding elevation of the curve for green light is 2 seconds. Since these values of crest time are characteristics of the red and green receptors respectively, this finding corresponds well with the sensory fact that at these intensities the specific sensations of red and green were evoked.
DISCUSSION It has long been taken for granted that the light-threshold is de termined by the excitation of rods alone.4)26-28) The present experiment has, however, shown that besides the so- called rod-process, the twin-process participates in achromatic twilight vision. The question now arises as to whether the two kinds of scotopic pro cesses distinguished by our method represent the two kinds of rods which were presupposed by some workers.34-3s) There is, however, no histologi cal evidence that in the human retina there exist two kinds of rods.17) It is certain that our so-called rod-process has all characteristics of rods, for example, 1. the spectral distribution of our rod-response coincides
78 T. Oikawa
Fig. 5. A: cone-system associated with rod. B: pure rod-system.
c: cones. r: rods. g, and g;: bipolar cells.
rod-process.
As mentioned above, retinal processes revealed by our method re-
present physiological events in the intermediate zone or retinal network.
Polyak provided histological evidence for convergence of cones and rods
into a common bipolar cell (see A in Fig. 5). In such a system the bipolar
cell would be excited by impulses initiated in the rod at the light-threshold,
because the visual purple contained in the rod may be considered more
sensitive to light than any cone-substance.") If the excitation process
of this bipolar is to correspond to the type of photopic processes, such a
system must exhibit dual behavior similar to that of the twin-process;
the spectral sensitivity of such a system will be determined by visual purple,
while the time constant of the excitation process will correspond to that
of cone-processes.
From this consideration it is very likely that the twin-process re-
presents the excitation of an intraretinal system receiving impulses both
from cones and rods (A in Fig. 5).
On the contrary, the rod-process may be considered to represent
the excitation of an intraretinal system receiving impulses from rods
alone (B in Fig. 5).
It has been shown above that the depression of either component of
the twin-process is associated with development of a color sensation when
the intensity is raised up to the color-threshold. Let us suppose a system
such as represented by A in Fig. 5 to be exposed to colored light of
intensity above the color-threshold. The bipolar gl will now receive im
pulses not only from the rod, but also from the cones, because the
intensity of light is sufficient to excite the cones as well.
Two Kinds of Scotopic Mechanisms 79
Since it is at the color-threshold or above it that one component of the twin-process drops out, the impulses from the cone must play some role in this phenomenon; in other words, inhibitory impulses started at the cone convert the colorless twin-process into a yellow or a blue process according to the wave-length of the light activating the cone in question. In this way a color process is released by inhibition. Needless to say, the color process so released will further be strengthened by active exci tation, and other color processes will also be activated when the intensity of light is raised further. The important part played by retinal inhibition in the formation of color sensations has been discussed by previous workers,40-42 and there are some physiological evidences for inhibitory processes in the retina .13-11)
SUMMARY Retinal processes were studied by the method of electrostimulation at 20? and 50? from the fovea.
- At the light-threshold there appear three processes of different time courses. The slowest one represents the excitation of rods. The other two processes correspond to the yellow and the blue process re spectively, judging from their crest times. Therefore, they are denoted by Y and B.
- At the light-threshold and in the photochromatic interval, the two processes, Y and B appearing always hand in hand, are equal to each other in magnitude and remain constant irrespective of the wave-lengths of illuminating lights. Therefore, they are called" a twin-process." This process subserves scotopic colorless sensations in conjunction with the rod-process.
- At the color-threshold, either Y or B component of the twin- process is depressed according to whether the wave-length of illuminating light is shorter or longer than 505 mƒÊ, but the other component remains intact. This finding corresponds to the psychological fact that at the color-threshold spectral lights give rise to yellow or blue sensation.
- The twin-process is a scotopic process having some properties similar to those of photopic processes. It differs from the rod-process in the following points; i) it originates in ofd elements or on/off-elements, ii) it exists only below the color-threshold, iii) its spatial distribution corresponds to the density distribution of cones, iv) its time constants are much shorter than that of the rod-process.
- The important role played by inhibition in the formation of color sensations is discussed.
I am greatly indebted to Prof. K. Motokawa for his many valuable dis-
Two Kinds of Scgtopic Mechanisms 81
1946, p. 151, cited from Hartridge, H., Recent advances in the physiology of the vision, London, Churchil, 1950, p. 28.
- Granit, R., Ergeb. Physiol., 1950, 46, 31.
- Motokawa, K., Ebe, M., Arakawa, Y. & Oikawa, T., Jap. J. Physiol., 1951, 2, 50.
- Wright, W.D., Researches on normal and defective colour vision, London, Henry Kimpton, 1946, p. 96.
- Gothlin, G.F., Upsala Lakareforen. Forhandl. N.F., 1943-44, 49, 433.
- Gothlin, G.F., Kungi. Svenska Vetenskapsakademiens Handlingar, Tredje Serien 1943, 20, No. 7.
- Householder, A.S., Psychol. Rev.,, 1947, 54, 169.
- Sherrington, C.S., The integrative action of the nervous system, New Haven, Yale Univ. Press, 1906, p. 208.
- Granit, R., Amer. J. Physiol., 1931, 98, 664.
- Granit, R., J. Physiol., 1933, 77, 207.
- Granit, R., J. Physiol., 1944, 103, 103.
- Granit, R. & Therman, P.O., J. Physiol., 1935, 83, 359.
- Granit, R. & Tansley, K., J. Physiol., 1948, 107, 54.
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