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RETINAL PROCESSING of VISUAL DATA* Generated in the Retina. The RETINAL PROCESSING OF VISUAL DATA* BY EDWARD F. MACNICHOL, JR. DEPARTMENT OF BIOPHYSICS, THE JOHNS HO6KINS UNIVERSITY, BALTIMORE, MARYLAND The experiments of the psychophysicists have shown with great precision what the human visual system is capable of doing, as Dr.. Judd has so ably summarized in this symposium. However, I am sure that none of us will be satisfied until we learn in detail how the seeming miracle of vision is accomplished. Throughout recorded history, man has sought to explain the workings of the eye, and in the last 150 years, progress has been made ht an ever-accelerating pace. The visual process of course starts with the focusing of a picture of the'outside world on the retina. By the end of the 19th century the main outlines of image formation in the eye were well understood, and at the present time the details are almost entirely filled in. However, the functioning of the retina has not been nearly as easy to elucidate. This year is the hundredth anniversary of the use of objective methods of studying retinal function, for it was in 1865 that Holmgren' reported that there is an elec- trical response to illumination of the eye and was able to show that the response is generated in the retina. The study of the visual pigments, begun slightly later by Boll and by Ktihne, has elucidated many facts in regard to their chemical nature and the reactions in which they participate, much of the key work in this area hav- ing been done in the laboratory of one of the participants in this symposium, Pro- fessor Wald. The pigments responsible for color discrimination have, until very recently, pre- sented us with an apparently insoluble problem. Although since the time of Thomas Young there has been overwhelming evidence of the trichromacy of nor- mal human vision, the pigments responsible for color vision have still not been separated and identified, presumably due to their instability, chemical similarity, and the difficulty of getting them into solution. Yet two key questions have to be answered before the earliest step in retinal analysis of color information could be understood: Are there three pigments which absorb light best in different parts of the spectrum in human cones, and are these segregated in separate receptors? Alternatively, are there three pigments mixed in a single kind of receptor which somehow responds in different ways depending upon which pigment absorbs the most light? A third possibility exists that there is only one pigment which is somehow distributed in the receptor in such a way that it is excited differently by different wavelengths of light. All of these possible mechanisms could give results which are equivalent by any psychophysical test. Therefore, it was necessary to use techniques which permit measurements to be made on the receptors themselves. Two techniques, micro- spectrophotometry and electrophysiology, appear to have given definite and un- equivocal qualitative answers to our question, though many quantitative details remain to be filled in. There are indeed three human cone pigments and each cone contains mainly, if not exclusively, one of these. Let us examine the evidence for this statement. That there is more than one photosensitive pigment in the human fovea was show a number of years ago by Rushton2 who, with Campbell, developed an in- 1331 Downloaded by guest on September 30, 2021 1332 MECHANISMS OF COLOR VISION PROC. N. A. S. a~~~I S -at,~ |- -,.Xa. ' e- ..- -I'- am a's all *a. ....... ..... ~as FIG. 1.-Plots of corrected bleaching-difference spectra of 28 isolated goldfish cones measured by passing light through the outer segments transversely to their axes. (From ref. 7.) strument that analyzed the light reflected from the back of the eye of a living hu- man subject after it had passed twice through the receptors. By measuring light of various wavelengths absorbed by the receptors before and after bleaching them with colored lights, he identified a green-absorbing pigment he called chlorolabe and a red-absorbing pigment, erythrolabe. He measured the pigment in protanopes, and showed that the erythrolabe was missing; and in deuteranopes, who were found to have no chlorolabe. Thus, he related color blindness to lack of pigment. Undoubtedly, the story of color blindness is not as simple as this, as Professor Wald's paper in this symposium makes evident; but Rushton clearly showed the existence of two different cone pigments and the lack of one or the other of them in some cases of color blindness. Similar experiments were performed on isolated excised foveas by Wald and Brown,I and by Ripps and Weale4 in the living eye with qualitatively similar results. Because of its small quantity and interference from the absorption spectrum of rhodopsin in neighboring rods, it was very difficult to demonstrate a blue-violet-absorbing pigment which is required by the trichromatic theory. Furthermore, experiments on populations of receptors could not answer the second part of the question: Are the pigments segregated into three kinds of receptors? Apparently, only measurements of absorption spectra or action of individual receptors could provide the answer. The problem was a formidable one because cone outer segments are very small and the pigments in them absorb atmostha few Downloaded by guest on September 30, 2021 VOL. 55, 1966 N. A. S. SYMPOSIUM: E. F. MAcNICHOL JR 1333 455 530 625 ... ._ . ..... ........ 4 0 . .- . ...... ^.-. ^ ,' . - . percentoftheincidenlight. Furthermore, the pigment is continu bbu l ref~7. re. 7.)** per cent of the inidn light. Futeroe the pimn is cotnal being FIG.e2.-Averagenbleaching-differncelcurveshobtainedibyedividingshedcuoe ishwlinmig.1 wvereintostremengousaei o detectand plottpingbleaohabldetheargei pigmetsofteainpthesgroupntsotereac segmensgroup atoeacothewaveengh.cotes (Fre-om-o ithe carhop.eThe c minno a spectra.-Measure-t absorpn specta andbeudesir in- instrumentblderachdblylagradtheemeasrinspnot fficie eihsense.dusirin , thebttheexeasriethnt.clarly deosrtoedthathacus oeofcns.Hw rFat measraemts wloueingd epossibesit atnique puwnwr thed totrvs limit. t imtesuoreenrsoaf rotdinthine te oueate, sgmekn ts fh rograos wh gh.areo istrumentwsntsier lnatrumespeilyfortisinlntrad therepupse.7tieease toWithitheueMlarkswayaltomoidentifyconets.fththreeu difraen kindreensofwonedinte gosildfish,ancanimalmveas knwneromthigmandtbeshavitora stdistoitHow-e veavraheiriSmounedyearshagoreslets menouragein isolaionorfithsedfitultieasmalpicthemt limgprove theirnofat hiqeretnad verythe sensJapan,rwith theahopeposestaWithsaTohimprovedyunusuallyeasurint wel-evhiqelBopedel-ehiqonae eslBown,5spectra.iMeanwhileandittabiitdtL iciiebadiscriminatreneeableMaksandcolors.tolos makteraccrae,Furtermcrae, iesreetscoesar largersthanthosofprmtes, semakngtheWysB.measurementds,cmdesieasiehr.onthed in- Thderisruetscrrnlyingrnuseeorearier all veasry siilrandhonsisofacourceHof- vaiablrue-wavpelength moochisromatic ligthmicMroscoeo whichbl theireceptortcell is mounted, either in isolation or in situ on a small piece of retina, a very sensitive photomultiplier tube, and an electronic recording system which compares the in- Downloaded by guest on September 30, 2021 13:34 MECHANISMS OF COLOR VISION PROCt. N. A. S. tensity of a beam of light which passes through the receptor to that of a reference beam which does not. Figure 1 shows a number of bleaching difference spectra of single goldfish (cones. The curves were scaled to the same peak height, corrected for bleaching of the light-sensitive pigment during the measurement, and plotted by a computer. It is evident that all but one of these curves fall into three groups. The odd one is the composite spectrum of a pair of twin cones and was rejected in the analysis of the results. Figure 2 shows curves, obtained by averaging the members of each of the three groups. The outer curves are standard deviations of the points, and the large spots are the absorptions of hypothetical rhodopsinlike pigments (the Dartnall nomogram) having maximum absorption at the same wavelengths as the peaks of the receptor curves.- As one can see, the agreement is quite good, so that it is unlikely that the pigments are of a very different composition from rhodopsin, the rod pigment, about which so much is already known. Liebman has repeated and confirmed these experiments independently, using a somewhat different method in which an absorption spectrum rather than a bleach- ing-difference spectrum is plotted. In addition, Tomita,8 in Japan, has obtained electrically recorded action spectra from single receptors of the carp, a species closely related to the goldfish. By mounting the retina on a vibrating plate, he was able to impale individual receptors with very fine micropipette electrodes. Figure 3 shows his results. The responses to light are negative or hyperpolarizing. The first response is to illumination of a very small area, the second is to illumination at the same intensity of a much larger area. The lower rec- ord (b) shows the so-called "S" potentials rec- orded from deeper in the retina. Illumina- a _ _ _ - tion of a large area gives a larger response than illumination of a small area, indicating that the "S" potential summates the responses of many receptors. The receptor potentials, on the other hand, appear to be area-insensitive as long as the illuminated region is larger than one receptor, as one might expect. This test quickly distinguishes a receptor response from the more easily obtained "S" potential; and as we shall see, the responses to different
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