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When single cones are stimulated with spots of 543-nm light presented against a white background, subjects report percepts that vary between predominately red, white, and green. However, light of the same spectral composition viewed over a large field under normal viewing conditions looks invariably green and highly saturated. It remains unknown what stimulus parameters are most important for governing the color appearance in the transition between these two extreme cases. The current study varied the size, intensity and retinal motion of stimuli presented in an adaptive optics scanning laser ophthalmoscope. Stimuli were either stabilized on target locations or allowed to drift across the retina with the eye's natural motion. Increasing both stimulus size and intensity led to higher likelihoods that monochromatic spots of light were perceived as green, whereas only higher intensities led to increases in perceived saturation. The data also show an interaction between size and intensity, suggesting that the balance between magnocellular and parvocellular activation may be critical factors for color perception. Surprisingly, under the range of conditions tested, color appearance did not depend on whether stimuli were stabilized. Sequential activation of many cones does not appear to drive hue and saturation perception as effectively as simultaneous activation of many cones.

The retina is the most accessible element of the central nervous system for linking behavior to the activity of isolated neurons. We unraveled behavior at the elementary level of single input units-the visual sensation generated by stimulating individual long (L), middle (M), and short (S) wavelength-sensitive cones with light. Spectrally identified cones near the fovea of human observers were targeted with small spots of light, and the type, proportion, and repeatability of the elicited sensations were recorded. Two distinct populations of cones were observed: a smaller group predominantly associated with signaling chromatic sensations and a second, more numerous population linked to achromatic percepts. Red and green sensations were mainly driven by L- and M-cones, respectively, although both cone types elicited achromatic percepts. Sensations generated by cones were rarely stochastic; rather, they were consistent over many months and were dominated by one specific perceptual category. Cones lying in the midst of a pure spectrally opponent neighborhood, an arrangement purported to be most efficient in producing chromatic signals in downstream neurons, were no more likely to signal chromatic percepts. Overall, the results are consistent with the idea that the nervous system encodes high-resolution achromatic information and lower-resolution color signals in separate pathways that emerge as early as the first synapse. The lower proportion of cones eliciting color sensations may reflect a lack of evolutionary pressure for the chromatic system to be as fine-grained as the high-acuity achromatic system.

In humans, experimental access to single sensory receptors is difficult to achieve, yet it is crucial for learning how the signals arising from each receptor are transformed into perception. By combining adaptive optics microstimulation with high-speed eye tracking, we show that retinal function can be probed at the level of the individual cone photoreceptor in living eyes. Classical psychometric functions were obtained from cone-sized microstimuli targeted to single photoreceptors. Revealed psychophysically, the cone mosaic also manifests a variable sensitivity to light across its surface that accords with a simple model of cone light capture. Because this microscopic grain of vision could be detected on the perceptual level, it suggests that photoreceptors can act individually to shape perception, if the normally suboptimal relay of light by the eye's optics is corrected. Thus the precise arrangement of cones and the exact placement of stimuli onto those cones create the initial retinal limits on signals mediating spatial vision.

Purpose: To develop and test the application of an adaptive optics scanning laser ophthalmoscope (AOSLO) with eye tracking for high-resolution microperimetric testing., Methods: An AOSLO was used to conduct simultaneous high-resolution retinal imaging and visual function testing in six normal subjects. Visual sensitivity was measured at test locations between the fovea and 5.0° eccentricity via an increment threshold approach using a 40-trial, yes-no adaptive Bayesian staircase procedure (QUEST). A high-speed eye tracking algorithm enabled real-time video stabilization and the delivery of diffraction-limited Goldmann I-sized stimuli (diameter = 6.5 arc min = ∼32 μm; λ = 680 nm) to targeted retinal loci for 200 ms. Test locations were selected either manually by the examiner or automatically using Fourier-based image registration. Cone spacing was assessed at each test location and sensitivity was plotted against retinal eccentricity. Finally, a 4.2 arc min stimulus was used to probe the angioscotoma associated with a blood vessel located at 2.5° eccentricity., Results: Visual sensitivity decreases with eccentricity at a rate of -1.32 dB/deg (R = 0.60). The vertical and horizontal errors of the targeted stimulus delivery algorithm averaged 0.81 and 0.89 arc min (∼4 μm), respectively. Based on a predetermined exclusion criterion, the stimulus was successfully delivered to its targeted location in 90.1% of all trials. Automated recovery of test locations afforded the repeat testing of the same set of cones over a period of 3 months. Thresholds measured over a parafoveal blood vessel were 1.96 times higher (p < 0.05; one-tailed t-test) than those measured in directly adjacent retina., Conclusions: AOSLO-based microperimetry has the potential to test visual sensitivity with fine retinotopic precision. Automated recovery of previously tested locations allows these measures to be tracked longitudinally. This approach can be implemented by researchers interested in establishing the functional correlates of photoreceptor mosaic structure in patients with retinal disease.

PurposeTo measure photoreceptor packing density and S-cone spatial resolution as a function of retinal eccentricity in patients with enhanced S-cone syndrome (ESCS) and to discuss the possible mechanisms supporting their supernormal S-cone acuity.MethodsWe used an adaptive optics scanning laser ophthalmoscope (AOSLO) to characterize photoreceptor packing. A custom non-AO display channel was used to measure L/M- and S-cone-mediated visual acuity during AOSLO imaging. Acuity measurements were obtained using a four-alternative, forced-choice, tumbling E paradigm along the temporal meridian between the fovea and 4° eccentricity in five of six patients and in seven control subjects. L/M acuity was tested by presenting long-pass-filtered optotypes on a black background, excluding wavelengths to which S-cones are sensitive. S-cone isolation was achieved using a two-color, blue-on-yellow chromatic adaptation method that was validated on three control subjects.ResultsInter-cone spacing measurements revealed a near-uniform cone density profile (ranging from 0.9-1.5 arcmin spacing) throughout the macula in ESCS. For comparison, normal cone density decreases by a factor of 14 from the fovea to 6°. Cone spacing of ESCS subjects was higher than normal in the fovea and subnormal beyond 2°. Compared to the control subjects (n = 7), S-cone-mediated acuities in patients with ESCS were normal near the fovea and became increasingly supernormal with retinal eccentricity. Beyond 2°, S-cone acuities were superior to L/M-cone-mediated acuity in the ESCS cohort, a reversal of the trend observed in normal retinas.ConclusionsHigher than normal parafoveal cone densities (presumably dominated by S-cones) confer better than normal S-cone-mediated acuity in ESCS subjects.

The human retina contains three classes of cone photoreceptors each sensitive to different portions of the visual spectrum: long (L), medium (M) and short (S) wavelengths. Color information is computed by downstream neurons that compare relative activity across the three cone types. How cone signals are combined at a cellular scale has been more difficult to resolve. This is especially true near the fovea, where spectrally-opponent neurons in the parvocellular pathway draw excitatory input from a single cone and thus even the smallest stimulus projected through natural optics will engage multiple color-signaling neurons. We used an adaptive optics microstimulator to target individual and pairs of cones with light. Consistent with prior work, we found that color percepts elicited from individual cones were predicted by their spectral sensitivity, although there was considerable variability even between cones within the same spectral class. The appearance of spots targeted at two cones were predicted by an average of their individual activations. However, two cones of the same subclass elicited percepts that were systematically more saturated than predicted by an average. Together, these observations suggest both spectral opponency and prior experience influence the appearance of small spots.