In a classic study, Kovács et al. [Proc. Natl. Acad. Sci. USA 93, 15508 (1996)] used an array of many disks presented dichoptically with half of the disks in one eye “red” and the other half “green;” disk chromaticities in the fellow eye were reversed, resulting in binocular color rivalry for every disk, thus creating color ambiguity. Surprisingly, the binocularly fused percept sometimes was all disks of the same color (red or green), which showed that perceptual resolution of the many ambiguous neural representations did not rely completely on monocular dominance or on independent resolution for each disk. The present study replicates and expands on the original with the aim to isolate binocularly driven neural mechanisms of perceptual resolution without contamination from monocular dominance. Observers viewed a color-rivalrous array with 16 disks presented either steadily to each eye, as in Kovács et al., or with chromatic interocular-switch rivalry (CISR), which swaps the two images between the eyes every 133 ms. The total proportion of viewing time when the 16 disks were perceived to be all red or all green was measured. For three observers, the disks all appeared the same color more often with CISR than with steady rivalrous presentation, suggesting that monocular dominance interferes with grouped perceptual resolution of ambiguous stimuli in the Kovács paradigm. This conclusion was supported by an additional condition using CISR, but with every disk the same color in one eye at each instant (e.g., all “red” disks in one eye and all “green” in the other). This condition was never significantly different from the original CISR condition, as expected if CISR reveals only binocularly mediated perceptual resolution of the disks’ color, irrespective of monocular neural representations. In conclusion, chromatically tuned binocularly driven neurons account for perceptual resolution of CISR.
Optoretinography (ORG) has the potential to be an effective biomarker for light-evoked retinal activity owing to its sensitive, objective, and precise localization of retinal function and dysfunction. Many ORG implementations have used adaptive optics (AO) to localize activity on a cellular scale. However, the use of AO restricts field-of-view (FOV) to the isoplanatic angle, necessitating the montaging of multiple regions-of-interest to cover an extended field. In addition, subjects with lens opacities, increased eye movements and decreased mobility pose challenges for effective AO operation. Here, we developed a coarse-scale ORG (CoORG) system without AO, which accommodates FOVs up to 5.5 deg. in a single acquisition. The system is based on a line-scan spectral domain OCT with volume rates of up to 32 Hz (16,000 B-frames per second). For acquiring ORGs, 5.5 deg. wide OCT volumes were recorded after dark adaptation and two different stimulus bleaches. The stimulus-evoked optical phase change was calculated from the reflections encasing the cone outer segments and its variation was assessed vs. eccentricity in 12 healthy subjects. The general behavior of ΔOPL vs. time mimicked published reports. High trial-to-trial repeatability was observed across subjects and with eccentricity. Comparison of ORG between CoORG and AO-OCT based ORG at 1.5°, 2.5°, and 3.5° eccentricity showed an excellent agreement in the same 2 subjects. The amplitude of the ORG response decreased with increasing eccentricity. The variation of ORG characteristics between subjects and versus eccentricity was well explained by the photon density of the stimulus on the retina and the outer segment length. Overall, the high repeatability and rapid acquisition over an extended field enabled the normative characterization of the cone ORG response in healthy eyes, and provides a promising avenue for translating ORG for widespread clinical application.
Light propagation in photoreceptor outer segments is affected by photopigment absorption and the phototransduction amplification cascade. Photopigment absorption has been studied using retinal densitometry, while recently, optoretinography (ORG) has provided an avenue to probe changes in outer segment optical path length due to phototransduction. With adaptive optics (AO), both densitometry and ORG have been used for cone spectral classification based on the differential bleaching signatures of the three cone types. Here, we characterize cone classification by ORG, implemented in an AO line-scan optical coherence tomography (OCT), and compare it against densitometry. The cone mosaics of five color normal subjects were classified using ORG showing high probability (∼0.99), low error (<0.22%), high test-retest reliability (∼97%), and short imaging durations (< 1 hour). Of these, the cone spectral assignments in two subjects were compared against AO-scanning laser opthalmoscope densitometry. High agreement (mean: 91%) was observed between the two modalities in these two subjects, with measurements conducted 6-7 years apart. Overall, ORG benefits from higher sensitivity and dynamic range to probe cone photopigments compared to densitometry, and thus provides greater fidelity for cone spectral classification.
A coherent percept of our visual world is important for functioning. Ambiguities, however, are implicit in visual neural representations and must be resolved for stable perception of objects and scenes. Grouping processes can link multiple neurally ambiguous fragments across the visual field. Experiments here determined how multiple visual features of each fragment contribute to perceptual resolution of ambiguity by grouping. Chromatic interocular-switch rivalry, a technique for presenting competing dichoptic images, was used to induce ambiguous neural representations for equiluminant chromatic discs and gratings. Two dichoptic stimuli were presented simultaneously to measure the amount of time they both appeared the same in at least one feature domain. The two stimuli were grouped when they appeared to share ambiguous features such as color, orientation, and spatial frequency more often than chance. Experiments here tested whether unshared and unambiguous features impeded grouping of the ambiguous components. Overall, the results show that grouping can be driven by neural ambiguity that is common for fragments across the visual field, even when the fragments also have other unshared, unambiguous features.
Competing rivalrous neural representations can be resolved at several levels of the visual system. Sustained percepts during interocular-switch rivalry (ISR), in which rivalrous left- and right-eye stimuli swap between eyes several times a second, often are attributed to competing binocularly driven neural representations of each rivalrous stimulus. An alternative view posits monocular neural competition together with a switch in eye dominance at the moment of each stimulus swap between eyes. Here, a range of experimental conditions was tested that would change the colors seen if mediated by eye dominance but not if by competition between binocularly driven responses. Observers viewed multiple chromatically rivalrous discs in various temporal and spatial patterns, and reported when all discs in view appeared the same color. Unlike typical ISR paradigms that swap the complete stimulus in each eye, some of the rivalrous discs were swapped at a different time, or faster frequency, than other discs. Monocular dominance of one eye at a time implies that all discs will rarely be seen as identical in color when some discs swap at a different frequency than others. On the other hand, competing binocularly driven neural responses are not affected by asynchronous swap timing among the individual discs. Results for every observer are in accord with competing responses at the level of binocularly driven, chromatically tuned neurons. Although an account based on eye dominance can be constructed using many small retinotopic zones that have independent timing for the moment of switching the dominant eye, competing binocularly driven responses are a more parsimonious explanation.
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