20  Post-receptor sensitivity regulation mechanisms

20.1  Psychophysical evidence

The close relationship between amount of bleached photopigment and sensitivity obtained during long-term dark adaptation strongly indicated that the sensitivity regulation mechanisms were mainly located in the receptors. Both Hecht and Wald had accepted this basic assumption. Rushton (1965a, b), however, strongly opposed this view. Thus, he held that both the signals from bleached photopigments and the signals generated by background light regulated sensitivity centrally to the receptors in what he termed ‘an automatic gain control-summation pool’ (AGC pool). He based his position on two different lines of evidence.

Firstly, he found that a background light so weak that less than 10% of the rods could have caught a single quantum of light raised the threshold three-fold. Apparently, the 10% of the rod receptors that had received a single photon hit had markedly reduced the sensitivity of the 90% that were quite unaffected by the adapting light.

Secondly, Rushton (1965a) could provide strong supporting evidence in favour of his view by both lightand dark-adaptation experiments.

In the light-adaptation experiment, Rushton took advantage of an ingenious technique where he stabilized the light stimuli on the retina. The background was a black-red grating of period 0.5º (presumed to be less than the receptive field of the summation pool) and the test flash, a black-green similar size grating (presumed to activate rod receptors). The test flash superimposed on the background was alternately inand out-phase.

The results showed that there was no threshold difference under these two conditions, supporting his view that the background

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light did not raise the quantum demand at the receptor level (i.e. the threshold for rod-receptor signals did not increase) and that all adaptation occurred at the pool.

This conclusion was also supported by experiments on dark adaptation where the bleaching light was sent by means of a brief electronic flash either through a grating of 0.5º period to give a striped bleach or through a neutral filter to pass an equal amount of light spread evenly on the retina. The test flash was under the latter condition a grating of 0.5º period, while it was an equalizing neutral test light in the former. Again, no significant differences between the two conditions were obtained.

Rushton (1965a) argued that if sensitivity regulation occurred at the receptor level, the dark bars of the grating should have shielded the retina from the flash of the bleaching light. The retina should thus have been fully dark adapted at the shielded regions, while every rod in the bleached area should have been substantially bleached when the same total bleaching light was evenly distributed on the retina. Hence, from his results he concluded that bleaching with the grating or with the same light spread evenly had about the same effect on the threshold level, and also that the threshold level obtained by the test flash was the same whether the test energy was concentrated by the grating or spread evenly – all in harmony with his AGC-pool hypothesis.

20.2  Anatomical and electrophysiological evidence

Anatomical and electrophysiological evidence supporting Rushton’s post-receptor adaptation theory was presented by Dowling (1967). Together with Boycott he had examined the synaptic organization of the retina in several types of vertebrate retina, including the primate, using an electron microscope. Striking support for Rushton’s AGC-pool hypothesis was obtained. Thus, they found widespread reciprocal synapses between bipolar cell terminals and amacrine-cell processes. The anatomical evidence indicated that bipolar cells made

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synaptic contacts with both ganglion-cell dendrites and amacrine processes, and that the amacrine processes made synaptic contacts back on to the bipolar terminal. The amacrine cell was found to make such reciprocal contacts with bipolar cells over wide areas in primates. Also, the amacrine cells were found to extend their processes throughout the inner plexiform layer and to make synaptic contacts with each other.

The reciprocal synaptic organization found would obviously be suitable for a feedback system as required by Rushton’s AGC model. Accordingly, Dowling (1967) suggested that activation of the amacrine process by the bipolar terminal might result in an inhibitory synaptic feedback on to the bipolar terminal, reducing the sensitivity of the bipolar cell in proportion to its excitation.

Dowling (1967) also found electrophysiological evidence in favour of a post-receptor adaptation site. Thus, he pointed to the study of Lipetz (1961, p. 639) who had found that illumination of one area in a receptive field of frog ganglion cells may raise the threshold in other areas of the receptive field – a result previously obtained in the classical study of the cat retina by Kuffler (1953). Furthermore, he found the b-wave of the electroretinogram, assumed to rise from bipolar cells, to be the first response in the visual system to show typical adaptation properties.

21  Rushton’s AGC model

21.1  Each receptor type has a separate and independent adaptation pool

Presupposing that the site of adaptation is located in summation pools situated centrally to the receptor level, one might expect that different kinds of receptor (rods, ‘red’, ‘green’ and ‘blue’ cones) would tend to interact in determining the adaptation process. In ­opposition to this view, however, Rushton (1965a) presented evidence suggesting that each class of receptor had a separate and independent AGC pool. Thus, he suggested that for rods and for each kind of cone the dependence­ of threshold on background and on bleaching were private, i.e. separate and independent.

Strong evidence in favour of independence between rod and cone adaptation pools was given by the well-known fact that the threshold level obtained during long-term dark adaptation may remain unchanged for several minutes during the cone-plateau period, while the sensitivity of the rods may increase by several log units. Indeed, with deep-red test light, the absolute threshold level of the cones may remain invariant for more than 20 min during the cone-plateau period before the rods eventually influence the threshold level. Furthermore, well-founded evidence in favour of the indepen­ dence of the adaptation pools for all the different receptor types was found by Rushton (1965a) in the extensive research work of Stiles on incremental threshold (see Stiles, 1978). This research work may be illustrated by Stiles’s well-known experiment together with Aguilar in 1954 on light adaptation of the rod mechanism. They briefly exposed a test stimulus in the extrafoveal retina superimposed on a steady, large adapting field. The threshold of the test stimulus was measured

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as intensity of the background field increased. They employed a blue-green test stimulus superimposed on a large red-adapting field to prevent cones from detecting the test stimulus. By this famous, so-called ‘two-colour threshold technique’, they were able to follow the incremental threshold of the isolated rod receptor system over most of its functional range before the cone receptors intruded.

Previously, Flamant and Stiles (1948) had provided strong evidence that the two-colour threshold technique could be used to isolate the rod receptor system. They had found that the reciprocal of the intensity of the adapting field required for different test wavelengths to raise the increment threshold by a fixed factor (1 log unit above the dark-adapted threshold) was very similar to the spectral sensitivity curve of the rod mechanism.

Stiles had obtained similar curves to the incremental rod curve under a variety of conditions intended to isolate the incremental curves of the different kinds of cone receptor. The results were judged to indicate that the different underlying adaptation mechanisms reacted independently of each other in that the most sensitive mechanism determined the threshold level except for a small probability summation factor operating when the two most sensitive underlying mechanisms approached equality (see Stiles, 1978). On this evidence Rushton (1965a) concluded that the different types of adaptation mechanism must operate independently of each other when threshold level is determined under light-adaptation conditions.

He then, in cooperation with Du Croz, investigated whether the different types of adaptation mechanisms also operated independently when threshold level was determined during dark adaptation(see Du Croz & Rushton, 1966). If so, they argued, it should be possible to obtain breaks in cone dark-adaptation curves similar to the breaks found in the incremental threshold curves obtained by the two-colour threshold technique and to the cone-rod break, by changing the relative sensitivity of the three cone-receptor types during dark adaptation. Their prediction was confirmed.