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Bleaches Are Substantial; Thus the Rapid Recovery Phenomenon Lies Outside the Conditions Here Examined

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Bleaches Are Substantial; Thus the Rapid Recovery Phenomenon Lies Outside the Conditions Here Examined 612 J. Phyaiol. (1965), 181, pp. a12-628 With 5 text-ftgure8 Printed in Great Britain DARK ADAPTATION AND INCREMENT THRESHOLD IN A ROD MONOCHROMAT By C. B. BLAKEMORE AND W. A. H. RUSHTON From the Physiological Laboratory, University of Cambridge (Received 30 April 1965) THE OBJECT The well-known fall in sensitivity of the eye when exposed to light and the subsequent rise in the dark has long been attributed to the bleaching and subsequent regeneration of rhodopsin and of cone visual pigments. This conjecture, held for thirty years without evidence, was shown to be on the right lines when Dowling (1960) demonstrated in rats that, after full bleaching, there was at each stage of regeneration a linear relation between the amount of rhodopsin in the retina and the log e.r.g. threshold at that moment. In man a quite similar relation was found between the log visual threshold measured in the usual way and the rhodopsin concen- tration measured directly upon the same area of retina by the technique of retinal densitometry. Though this result could be inferred with some confidence from work on normal eyes (Rushton, 1961a) it was displayed more clearly in the eye of a special subject (Rushton, 1961 b) who lacked nearly all cone vision but whose rhodopsin and rod vision appeared quite normal. If the threshold is expressed in units of the fully dark-adapted value, the relation found was that log threshold is proportional to the amount of rhodopsin bleached. But, as was pointed out in the brief Discussion of the previous paper (Rushton, 1961 b), there are two respects in which this simple relation fails. (a) If the brief adapting light bleaches only a small fraction of rhodop- sin, visual sensitivity recovers rapidly, and all agree that the process is in some way different from that linked to the slow regeneration of rhodopsin after substantial bleaching. In the present paper, as in the former one, all bleaches are substantial; thus the rapid recovery phenomenon lies outside the conditions here examined. (b) The simple relation found that log threshold was proportional to the amount offree opsin could not be quite right. To be sure, something changes uniquely with the rhodopsin concentration and may affect the threshold in the way described, but it is not the threshold itself that stands in unique relation to pigment concentration. For several workers have shown that threshold depends also upon the kind of test flash used to measure it. In DARK ADAPTATION IN A ROD MONOCHROMAT 613 his last paper Lythgoe (1940) discussed dark adaptation with great insight and pointed out that something like a reorganization of nerve connexions must play an important part. Craik & Vernon (1941) measured the visual threshold during dark adaptation using either large or small test flashes and found quite different shapes for the corresponding dark adaptation curves, confirmed by Crawford (1947) and Arden & Weale (1954). Wolf & Zigler (1950) placed an acuity grating in the test flash and found that the shape of the resulting dark adaptation curve depended upon whether the threshold task was to see the flash or to resolve the grating. These results were confirmed and extended by Brown, Graham, Leibowitz & Ranken (1953). There would of course be little difficulty in reconiciling these obser- vations with the unique dependence of dark adaptation upon the regenera- tion of rhodopsin, if a change in the nature of the test flash did nothing more than shift the log threshold curve bodily up and down. But all investigations have shown that not only the position but the shape of the dark adaptation curve alters and that the range of the log threshold change for a given bleach depends upon the criterion by which the threshold is measured. It is plain that we should be faced with a heavy task in explaining the way in which adaptation depends upon rhodopsin bleaching if first we had to explain how threshold depends upon the varied criteria which may be used in its measurement. Fortunately as long as thirty years ago views were being advanced which suggested a great simplifica- tion of the problem. Holladay (1926, 1927), Stiles (1929, 1930) and others worked upon the effect of glare-the change in properties of one region of the retina when a distant region of small area is brightly illuminated. They found that the effect was as though a luminous veil was spread over the test field, and they measured this equivalent luminance by replacing the glare by the uniform veil that produced identical results. 'There is actually such a veil due to the diffusion of light within the eye, but it explains only a part of the phenomenon and the remainder is a fictitious luminance which represents [retinal] inhibition' (Le Grand, 1957). The tentative conclusion reached at that time was that there is a 'state of adapta- tion' of the retina which could result from various conditions (e.g. either from a uniform veil or from a distant localized glare), and the properties of the retina appeared to depend upon its state of adaptation but not upon the particular conditions which produced it. Lythgoe & Tansley (1929) (see also Lythgoe, 1940, fig. 2) investigated the flicker fusion frequency using a small flickering patch of fixed intensity with a luminous surround. They either varied the intensity of the surround or they light-adapted the eye and followed the critical fusion frequency (CFF) throughout the subsequent dark adaptation. In a general way it appeared that, for each intensity of flickering light, the effect upon CFF 614 C. B. BLAKEMORE AND W. A. H. RUSHTON of light adaptation was the same as the effect of some bright surround, and, as dark adaptation proceeded, the CFF results were as though the surround was progressively dimmed. If these thirty-year-old ideas are true we need not bother about the complex way in which threshold depends upon the parameters of the test flash, in our attempt to relate bleaching to adaptation. It is only necessary to find the luminance that is equivalent by one criterion of threshold, and it will be equivalent by all others. 'Threshold' drops out of the picture and the equivalent luminance that remains is the retinal state that should stand in unique relation to bleaching. But how true are those ideas, and in particular how well is dark adaptation represented at each stage by some equivalent luminance whose value is independent of the criterion by which it is measured? The most complete and accurate comparison is that ofCrawford (1947), where the increment threshold of a flash upon various intensities of back- ground is compared with the threshold in dark adaptation at various times following an exposure which he has told us amounted to 20,000 troland seconds of retinal illumination. The area of test flash was the same in each pair of experiments, and in different pairs it varied between 0.180 and 5.70 in angular subtense. What Crawford found was that, if dark adapta- tion is plotted not as log threshold against time but as log equivalent luminance against time, the curve is very nearly the same, independent of the area of test flash used. The experiments, however, were undertaken for certain practical ends and have three imperfections from the present academic view-point. First; there was no fixation point provided, so the subject used whatever part of the retina suited him best at the moment, and no doubt this lay closer to the central fovea the more the eye was light adapted and the smaller the test flash. Second, no attempt was made to separate rod thresholds from cone thresholds, and, since in general the equivalent luminance of dark adaptation cannot be the same for rod and for cone vision, the exact relation was somewhat obscured. Third, the bleaching was certainly not substantial; it was only about 0*2 % of the total amount of rhodopsin present. If rhodopsin is bleached by an exposure (It) troland sec applied for less than 1 min (so that re- generation is very small; Campbell & Rushton, 1955), then the fraction p of the initial pigment that remains unbleached is given (to good approxi- mation) by loglologlo(I/p) = log1o (It)-7.3. (1) This formula is derived from the assumption that the rate of bleaching (-dp/dt) is always proportional to the rate at which quanta are being absorbed (kpI), and it has been shown to hold for rods (Rushton, 1956) DARK ADAPTATION IN A ROD MONOCHROMAT 615 and for cones (Rushton, 1958, 1963a, 1965a). The figure 7*3, which applies to rods only, is derived from measurements of the rate of bleaching of rhodopsin in normal eyes (Rushton, 1956). Crawford's log (It) was 4 3, thus log I/p = 0.001 and the fraction bleached was 0-0023. The minute extent of the bleaching in Crawford's experiments does not detract from their importance in demonstrating that the subsequent stages of recovery may each be represented by a background whose equivalence is valid no matter what size of test flash is used. But without further in- vestigation we may not conclude that this principle of 'equivalent lumin- ance' applies to the quite different kind of adaptation that is linked to rhodopsin; for that requires the substantial bleaching of rhodopsin that Crawford did not employ. In the present paper, therefore, we have repeated some of Crawford's experiments, using large bleaches, and following the subsequent adaptation over a millionfold range of thresholds. This is not possible with normal subjects but one of us (Rushton, 1961b) has shown in experiments upon a subject with very little cone function that rod dark adaptation and incre- ment threshold can be measured over a range of about 6 log units, using large test areas.
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