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For example, bleaching the ‘red’ and ‘green’ cone photopigments completely with an orange light that was hardly absorbed at all by the ‘blue’ cone photopigment was found to favour the sensitivity of the ‘blue’ mechanism to such an extent that it could be measured in isolation with a blue test light during the first 90 s of the darkadaptation period. Thereafter, the sensitivity of the ‘green’ cone mechanism was found to surpass that of the ‘blue’ producing a break in the dark-adaptation curve.

Similarly, by selective chromatic adaptation, breaks between the ‘red’ and ‘green’ cone dark-adaptation curves could be obtained, and isolated ‘red’ and ‘green’ branches could be plotted in their entirety.

On this evidence Du Croz and Rushton (1966), in harmony with Stiles’s hypothesis that the four receptor-adaptation mechanisms acted independently in increment threshold measurements,­

suggested that they also acted independently of each other during dark adaptation. Thus, the apparent independence of the dark-­adaptation curves found for the four receptor mechanisms was assumed to imply separate and independent AGC organization: for each of the four dark-adaptation mechanisms the threshold was thought to be determined only by its own photopigment and its own AGC pool (see Rushton, 1965a).

21.2  Are light and dark adaptation really equivalent?

The similarity between light and dark adaptation found could easily be accounted for if they were based on the same underlying mechanism. To address this problem, Rushton made an extensive investigation to determine whether light and dark adaptation were, in fact, equivalent (see Rushton, 1965a).

The concept of equivalence of visual adaptation had been analyzed previously in a remarkable paper by Stiles and Crawford (1932) where they also put forward a test of equivalence: if two different adaptation procedures caused the same state of adaptation,

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then a given test stimulus should produce the same perception under the two procedures irrespective of the nature of the test.

The test of equivalence between dark and light adaptation had been carried out and confirming results had been obtained by both Crawford (1947) and Blakemore and Rushton (1965). Thus, both studies had found that variation in test parameters that produced marked changes in threshold level during dark adaptation produced the same changes in threshold level with light adaptation.

21.3  A decisive experiment

Yet, Rushton (1965a) was not quite convinced and therefore made an additional, so-called decisive test of equivalence, where he investigated whether the spatial organization of the adaptation pool for bleaching and light signals was the same. In this experiment, he measured dark-adaptation and incremental-threshold curves with the interposition of a perforated plate in front of both the bleaching and background lights. The holes of the plate were in sharp focus on the retina subtending an angle of about 0.5º from hole to hole.

The results showed that the dark and light adaptation produced vastly different adaptation effects: with dark adaptation, the log threshold elevating effect was found to be proportional to the average amount of bleached photopigment while with light adaptation the desensitizing effect (the increase of test intensity) was proportional to the average luminance of the background light confirming his general rule that the threshold is raised simply by the average light flux independent of spatial distribution (within the summation area) of the background light. Apparently, there had to be a marked differ­ ence between the spatial spread of the desensitizing influence of real and ‘dark’ light. Consequently, Rushton (1965a) concluded that lightand dark-adaptation processes were not equivalent.

To describe the two different processes, he developed his AGC model in more detail (see Rushton, 1965a, b). Thus, he assumed that the background-light signal when entering the input of the gain box became logarithmically transformed as indicated by Fechner’s famous law:

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S = k log R,

i.e. magnitude of sensation (S) is logarithmically related to magnitude of stimulus (R). The transformed signal, then, was thought to be fed back to the gain box and to summate with the bleaching signal. Finally, this summed signal was thought to affect log threshold level linearly.

21.4  The adaptation mechanisms explored by the after-flash technique

Rushton (1972) presented an important further development of his model of light and dark adaptation. Together with Alpern and Torii he explored the adaptation processes by a new ingenious psychophysical technique. Thus, they adapted the test field area by presenting a contrast light flash φ and a steady background field θ in a surrounding annulus area. (Another background field could be presented in the test area.) The light flash φ was presented shortly after a test flash λ had been exposed.

Both φ and θ were found to increase the threshold level of the test flash λ and, hence, to reduce the sensitivity of the test area. This reduced sensitivity was assumed to be determined by an ­inhibitory nerve signal N. Presupposing that N would remain constant under conditions where the test flash λ was kept fixed at a certain intensity level and reduced perceptually just to threshold level by φ and/or θ, they could vary intensity of φ and θ for a constant inhibitory N-signal, and by repeating this procedure for other fixed intensity levels of the test flash λ, they could establish the ­relationship between all the three variables. In this way they obtained the following formula:

N = [φ/(φ + σ)] • [θD/(θD + θ)]

where σ is the so-called semi-saturation constant, i.e. the intensity of φ that raises N to half its maximum, and θD is the intrinsic light of the eye (‘dark light’) that may be seen when the eye is in a completely dark-adapted state.

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The formula was found to hold for a large range of N, φ and θ variations and was therefore considered to be of fundamental importance for the understanding of the adaptation processes.

One important achievement of the formula was that it provided a quantitative explanation of receptor saturation like the saturation Aguilar and Stiles (1954) had found for the rod receptor. Previous evidence had indicated that there existed a basic difference between rod and cone background adaptation in that the rod response saturated when only a small fraction of rhodopsin was bleached, while the incremental threshold of the cones could be followed to very high background intensity levels where nearly all the cone pigments were bleached and yet showed no upward turn away from the straight Weber law incremental threshold behaviour that would indicate the start of the saturation process.

Their formula, on the other hand, predicted saturation both for rods and cones. Thus the equation shows that however great φ becomes, N will never reach [θD / (θD + θ )].

They performed a test that confirmed the prediction: cone saturation occurred as expected when a background light was presented only briefly – at a time when the increment φ was flashed upon it. Thereby the bleaching of the cone pigment was slight and the threshold rise could be obtained almost uncontaminated by any impoverishment of quantum catching through bleaching. The reason for previous failures to obtain cone saturation was thereby revealed: cones at high background intensities bleach much more quickly than rods. As a consequence, in attempts to demonstrate cone saturation under background equilibrium or so-called steady state conditions, much of the cone pigment is bleached away so that the capacity for absorbing light quanta becomes smaller, limiting the adaptation effect of the background light.

An interesting extension of their data was obtained by bleaching the photopigment in the annular surround to various degrees. They could then compare the test threshold-elevation effect of bleaching

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and steady background adaptation procedures. No equivalence was found. With background adaptation the semi-saturation constant σ remained invariant, whereas with bleaching adaptation it increased. These results, then, further strengthen the suggestion that background and bleaching adaptation were fundamentally different.

21.5  Limitations of Rushton’s photochemical theory

Previously, both Rushton and Dowling had provided strong evidence that long-term dark adaptation was controlled by photochemical processes. Both had found that log rod threshold was proportional to the amount of bleached rhodopsin, i.e. log T = cB. Serious problems, however, soon became apparent. Rushton (1972) pointed out two important limitations: (1) rod responses to light could not be registered before 50% of the rhodopsin had regenerated (as Granit, 1938, 1939 had shown), (2) when the adapting light bleached less than 10% of rhodopsin, the threshold level was found to be raised and to fall far more than expected on the basis of the Dowling-Rushton equation during the early phase of dark adaptation.

Rushton (1972) and Rushton and Powell (1972a, b) attempted to account for these limitations in line with the conclusions previously reached by Donner and Reuter (1968). These authors had obtained results with frogs that suggested that accumulation of meta II (a photoproduct of rhodopsin not yet degraded to leave free opsin) caused rod saturation under light adaptation, and that the decay of this photoproduct determined the first rapid phase of recovery during rod dark adaptation. Similarly, Rushton presumed that meta II produced strong afterimages and caused the observed deviations between the Rushton-Dowling formula and the actual threshold measurements. However, about 5 min after a strong bleach, the amount of meta II and free opsin were assumed to reach a state of equilibrium and thereafter to be proportional to each other, so that they both remained proportional to the log threshold elevation. He found supporting evidence for the photochemical explanation of dark adaptation in that the

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never able to decide what the relation was. His insistence upon the hopeless attempt to make a single kinetic system explain such utterly divergent adaptations as that from bleaching and that from backgrounds has thrown the whole subject into a lasting confusion.

Not only the kind of mechanism of bleaching and background adaptation, but also their sites of adaptation were assumed to be different. Thus, Rushton (1972) had come to suspect that bleaching adaptation was mainly sensitivity regulation in the receptors, while background adaptation was mainly a signal scaling mechanism proximal to the receptors – possibly situated in the horizontal cells. He found supporting evidence in the immense number of receptorbipolar junctions these cells connected to. On p. 505 Rushton (1972) made his position clear, ‘For eight years I have hoped that the horizontal cells are Fechner scalors, and I still hope so.’