22  Contribution of H. B. Barlow

22.1  Dark and Light adaptation based on similar mechanisms

In contrast to the assumption of Rushton that light and dark adaptation were determined by quite different mechanisms, Barlow (1964) put forward the hypothesis that their underlying mechanisms were very similar; that the sensitivity regulation during dark adaptation was mainly determined by so-called ‘photon-like’ events. Thus, he presumed that the presence of bleached photopigment caused the receptors to show effects similar to those induced by light. Both the bleached photopigments and light increased the intrinsic noise level of the receptors. In fact, the effect of bleached pigments was assumed to add to that of light so that the separate effects of the two factors could not be distinguished at the receptor output.

22.2  Both noise and neural mechanisms involved

There was, however, a serious obstacle to Barlow’s noise theory, since the expected square root law was not fulfilled in incremental threshold measurements. Thus, if a light flooding the retina elevated the threshold solely by virtue of the intrinsic noise level of receptors (i.e. the statistical fluctuation in the number of quanta absorbed) the incremental threshold should rise in proportion to the square root of the intensity of the flooding light (see De Vries, 1943; Rose, 1953; Barlow, 1957). Opposed to this prediction, however, it had been found that, over a large range of background intensities, the incremental threshold for a large test field rose in direct proportion to the background intensity (the Weber law). Only for small test targets and moderate background intensities were the expectations fulfilled.

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On this evidence, Barlow had to conclude that, in addition to the noise factor, another factor was involved causing the threshold to rise faster than simple noise consideration would have led one to expect.

22.3  Evidence in support of the noise theory

In 1972 Barlow re-evaluated his noise theory. He agreed with Rushton (1965a) that the relation between the amount of bleached rhodopsin and rod threshold during long-term dark adaptation was given by the well-known Dowling-Rushton formula (log T = c B), and that the threshold level measured during the dark-adaptation period, therefore, was somehow determined by the amount of bleached photopigment. If this suggestion were correct, there had to be a very rapid increase of the desensitizing reaction with a rise in the amount of rhodopsin bleached; the reaction would have to depend exponentially upon the concentration of bleached rhodopsin. No mechanism that could explain this reaction had yet been demonstrated, but Barlow argued that the receptors were structures with a high degree of organization, and that, therefore, a small proportion of altered molecules might cause disproportionately large effects. Bleaching a single molecule might significantly change the condition of other molecules in its vicinity, and cooperative action of this kind might give rise to an exponential law (Barlow, 1964).

Opposed to the suggestion of Rushton, however, that the darkand light-adaptation mechanisms were fundamentally different, Barlow stressed the similarity, suggesting that dark and light adaptation were equivalent processes. Thus, he suggested that receptors in the dark, containing a proportion of bleached photopigment, signalled messages indistinguishable from those caused by the illumination of the receptors. The so-called ‘dark’ and real lights, therefore, had the same adaptation effect; they both enhanced the noise level of the receptors and, thereby, reduced their sensitivity.

He found supporting evidence in the results obtained by Crawford (1947) and Blakemore and Rushton (1965), who had

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demonstrated that variation in the test parameters that produced marked changes in threshold level during dark adaptation produced the same changes in threshold level under light-adaptation conditions. These results, then, passed the test of equivalence put forward by Stiles and Crawford (1932).

Yet, Barlow found an even more striking confirmation of the noise theory in the results obtained by Barlow and Sparrock (1964). They had shown that when the brightness of a background light under stabilized conditions matched the brightness of the positive afterimage obtained at any particular moment during long-term dark adaptation, the incremental threshold level of this background brightness was the same as the threshold level measured during dark adaptation at that moment. This result, of course, nicely fitted the view that the positive afterimage represented ‘dark light’ equivalent to real light with regard to adaptation.

22.4  Opposing evidence

Barlow (1972) also considered evidence that opposed his adaptation theory. He found that although some of this evidence might be surmountable, important objections remained. Firstly, Rushton (1965a, b) in his so-called decisive experiment had demonstrated that bleaching the retina with an array of small light dots and adapting the retina with a similar array of luminous dots produced vastly different adaptation effects, indicating that there was a marked difference between the spatial spread of the desensitizing influence of real and ‘dark’ light.

This suggestion was further strengthened by Westheimer (1968) who found that real but not ‘dark’ light could produce the sensitizing effect first demonstrated by Crawford (1940). Thus, he found no evidence of sensitizing interaction between test spots and annuli composed of real and ‘dark’ light, respectively.

Also, opposing ­electrophysiological evidence had been forth­­ coming. Thus, Cone (1963/1964) had found that the latency of the b-wave of the rat electroretinogram was not affected equally by

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bleaching and background light, and Naka and Rushton (1968) had found that background light, but not bleaching, produced a steady hyperpolarization of the intracellular recorded S-potential.

Moreover, psychophysical measurements had shown that the log difference between incremental threshold curves obtained with large, long duration test flashes and those with small, brief test flashes was markedly reduced as background intensity was increased. Barlow (1972, p.10) concluded:

Clearly changes of performance of this sort cannot result solely from photochemical bleaching or alterations of receptors, and must involve changes in the neural mechanism. The loss of summation ability at higher backgrounds is accompanied by improved resolution; it is as if the retina changed to resemble a finer grain film being operated at a faster frame repetition frequency at higher luminance.

Similar conclusions had previously been reached by Granit and Lythgoe (see Granit, 1947; Lythgoe,1940).

Thus, although his original theory had received striking confirmation from several sources, Barlow (1972) acknowledged that neural-adaptation mechanisms had also to be taken into account to explain adaptation processes.

Another potential complication was that the human retina contained both rods and cones and that the cones were of three different kinds. Yet, Barlow (1972) obtained a great simplification by accepting Du Croz and Rushton’s (1966) suggestion that Stiles’s ‘red’, ‘green’ and ‘blue’ cone mechanisms with regard to threshold determination operated nearly independently of each other, both under bleaching and background adaptation conditions.

22.5  Sensitivity difference between rods and cones explained

In his summary paper, Barlow (1972) also attempted to explain the marked difference known to exist between rod and cone sensitivity.

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Three different contributory factors were mentioned: (1) the ‘dark light’ of rods was generally much lower than that of cones, (2) rods had a much greater spatial and temporal summation capability due to the properties of neural connections between receptors and ganglion cells (by improving the conditions for spatial and temporal summation maximally, the relative sensitivity difference between rods and cones may increase by more than 1 log unit), and (3) the rhodopsin of rods had a greater total optical density than the cone photopigments. The latter factor, however, was assumed to play only a minor role.