8 The duplicity theory of R. Granit
The spikes recorded by Hartline and Kuffler with the microelectrode technique represented end products in a series of consecutive events in the retina, starting with absorption of photons. To gain information about these extremely complex events that preceded the discharges of the optic nerve fibres, the research workers had to rely on the measurements of the electroretinogram (ERG). Indeed, it was generally held that mechanisms underlying the ERG response directly determined the impulse pattern of the optic nerve.
The ERG technique was first employed in 1865 by Frithiof Holmgren, a Swedish physiologist. He applied a pair of electrodes to an eye and found that the galvanometer connected to the electrodes gave a marked deflection both when the eye was illuminated and when the light was turned off. (For a description of the development of this technique, see introduction section of Granit, 1963.)
8.1 Supporting evidence for the duplicity theory from the ERG technique
A very extensive review of the research literature on ERG was made by Granit (1947). Presuming that the ERG response represented an average reaction, reflecting the processes of activated photoreceptors, the evidence reviewed was found to support the duplicity theory, suggesting that there were two quite different ERG response patterns of the retina, the so-called E- and I-ERG responses – the former characteristic of rod-dominant and the latter of cone -dominant retinas.
The hypothesis that the ERG response of rod and cone retinas differed was based on evidence obtained by measuring the ERG under conditions where the relative contribution of the two receptor types
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Fig. 8.1 A typical ERG curve as obtained by Granit (1938) with the multi -phasic fluctuation of potential; the characteristic a-, b-, c- and d-waves. These electrical changes have been analyzed by Granit into three components, PI, PII and PIII, as shown in the figure.
was varied, for example, by lightand dark-adapting the eye, by using retinas of different species where the relative number of rods and cones varied, and by using blue and deep red test lights. The most convincing evidence in favour of the hypothesis was obtained under conditions where the adaptation level of the eye changed. Thus, during long-term dark adaptation, for example, the ERG of a mixed rod-cone retina underwent both a Purkinje shift (the maximum spectral response changed from about 560 nm to about 500 nm) and a change from the I- to the E-ERG response.
The ERG of an E-retina containing both rods and cones is illustrated schematically in Fig. 8.1 where both the different waveforms (a, b, c and d) and the presumed underlying components (PI, PII and PIII) are shown. All these underlying components were found to be present in both types of retina, but to different degrees.
The ERG of the I-retina was characterized by marked a- and d-waves, assumed to be determined by the underlying PIII component, representing a rapidly reacting negative electrical potential. To account for this characteristic of the I-retina, Granit (1947) assumed
80development of the duplicity theory from 1930–1966
that the cone system, in contrast to the rod system, made extensive contacts with amacrine cells that distributed inhibition in the retinal pathways.
The ERG response of the E-retina, on the other hand, was characterized by a marked b-wave, assumed to reflect the underlying slow-reacting excitatory electrical potential PII that excited the nerve fibres and produced their ‘on’ responses.
The c-wave (the slow secondary rise of the ERG) was supposed to be determined by the PI component, but Granit (1947) presumed that this component either did not affect the discharge of the nerve fibres at all or did so indirectly by altering the threshold level of the discharge.
Granit found further support of his explanation of the E- and I-retinas when he measured the change in the ERG response with light adaptation both in an E-retina containing rods and cones and in a pure I-retina containing only cones. Thus, while the E-retina showed a decrease in the b-wave (indicating a reduction of the excitatory PII underlying component) and a relative increase in the a- and d-waves (indicating a relative increase of the inhibitory PIII component), the pure I-retina showed no appreciable change in the form of its ERG.
He obtained another supporting finding with important theore tical implications under conditions where the light stimulus was flickering. In the E-retina the flickering light stimulus produced a sequence of b-waves (b-b-b-b-b), while the I-retina elicited alternating a- and b-waves (a-b-a-b-a-b). Also, the I-retina was able to follow a much higher flicker rate than the E-retina, presumably due to the rapidly reacting inhibitory PIII component that dominated theI-retina response. Accordingly, while the pure E-retina, containing no cones, would tend to elicit simple, relatively slow ‘on’-responses in the nerve fibres, the I-retina would be able to produce complex, rapidly changing ‘on-off’ discharges.
Granit (1947) presumed that this characteristic of the I-retina gave extreme efficiency in transforming a visual field into frequency codes that could carry information about the physical world to the