Cone-specific mediation of rod sensitivity in trichromatic observers

Abstract

PURPOSE. The slope of the rod threshold versus the illuminance (TVI) function changes with the wavelength of the background light. This study was conducted to determine whether the changes in slope are due to the stimulation of specific cone classes. METHODS. An eight-channel optical system was used to generate lights that differed in cone and rod photoreceptor illuminance. Rod flicker TVI functions were measured in normal trichromatic observers at mesopic light levels. The independent variables were (1) the relative contribution of the short (S)-and long (L)-wavelength cones to the background light (i.e., the background lights varied along S-only and L-only lines), and (2) the temporal frequency of the flickering lights (4, 7.5, and 15 Hz). RESULTS. The 4-Hz rod flicker TVI function had a slope of 0.87 when measured near W (MacLeod-Boynton chromaticity of 0.66, 1.0). At 4 and 7.5 Hz, an increase in the relative L-cone illuminance steepened the slope of the rod-only TVI curve, but an increase in the relative S-cone illuminance had no effect. The slope of the 7.5-Hz TVI function decreased at higher illuminance levels. At 15 Hz, the thresholds could be measured over only a limited range. CONCLUSIONS. The L-cone system contributes to the desensitization of the rod system at mesopic light levels, whereas, in the range of lights used in these experiments, the S-cone system apparently does not. The possibility that S-cone stimulation desensitizes the response to rod signals at higher levels of S-cone illumination cannot be eliminated. (Invest Ophthalmol Vis Sci. 2002;43:898 -905) T he primate visual system operates over a range of 10 log units. This ability is due in part to the duplex retina in which scotopic (i.e., rod-dominated) vision operates at low light levels and photopic (i.e., cone-dominated) vision operates at high light levels. In several early studies, researchers proposed that these two systems behave independently of each other under many conditions, 1-4 but there is now clear evidence of the rods' influence on the cone systems and the cones' influence on the rod system. Visual signals originating in the rod photoreceptors do not have their own pathway to the brain but instead combine with neural signals originating in the cone photoreceptors. Signals originating with the rod photoreceptors are transmitted to the retinal ganglion cells through at least two anatomic pathways. One pathway combines through second-order cells. Rod photoreceptors connect to rod bipolar cells, which in turn connect to rod (AII) amacrine cells. The rod amacrine cells have gap junction connections with on-center ganglion cells in sublamina b of the inner plexiform layer, and have inhibitory synapses with off-center ganglion cells in sublamina a. Rod signals may also enter the cone circuit through gap junctions between rod spherules and cone pedicles (see Refs. 5-7). There is also recent evidence in rodents of a third pathway connecting the rod photoreceptors directly to OFF cone bipolar cells. 8,9 The general perceptual consequences of interaction between rods and cones have been documented extensively. We know, for instance, that the rod photoreceptor system influences cone-mediated sensitivity 10 -13 and vice versa 14 -18 ; that interaction between the rod and cone systems is more evident with flashed lights than with steady lights 19 ; and that location, spatial extent, and temporal frequency play an important role in determining the magnitude of rod and cone interaction. 17,20 -24 Rod-cone interaction (how rods influence cones) and cone-rod interaction (how cones influence rods) have become umbrella terms that characterize many classes of visual processing. One historical difficulty with experiments that investigate rod-cone (and cone-rod) interaction is that the narrowbandwidth lights (i.e., lights of a few spectral wavelengths) used as experimental stimuli often stimulate more than one class of photoreceptor. These experiments therefore do not lend themselves as easily to physiological interpretation. Many previous researchers have addressed such topics by measuring rod sensitivity to lights to which the rod system is much more sensitive than the cone systems (e.g., Ref. 25) or by investigating the responses of monochromatic and dichromatic observers. 26 -28 To investigate questions concerned with cone-rod interaction, I used an approach based on the cone-rod photoreceptor space defined by Shapiro et al. For this article, I examined rod TVI functions for 4-Hz flickering lights. Aguilar and Stiles 25 measured a rod TVI function by optimizing experimental parameters to isolate the rod system. One of these optimizations was to desensitize the cone systems with a long-wavelength adaptation light. They found that the slope of a major portion of the curve (i.e., when the adaptation light is between Ϫ2 and 2.2 log scotopic trolands [td]) is approximately 1.0. However, Sharpe et al

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