Human gaze is systematically offset from the center of cone topography

• Published in: Current biology 2021-09, Vol.31 (18), p.4188-4193.e3
• Main Authors: Reiniger, Jenny L., Domdei, Niklas, Holz, Frank G., Harmening, Wolf M.
• Format: Article
• Language: English
• Subjects: adaptive optics; binocular; fixation behavior; foveola; psychophysics; visual field
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.07.005

The small physical depression of the human retina, the fovea, is the retinal locus of prime visual resolution, achieved by a peaking topography of the light-sensitive cone photoreceptor outer segments1–3 and a post-receptor wiring scheme preserving high-density sampling.4,5 Humans dynamically direct their gaze such that the retinal images of objects of interest fall onto the foveola, the central one-degree diameter of the fovea,6–8 but it is yet unclear whether a relationship between the individual photoreceptor topography at this location and visual fixation behavior exists.9,10 By employing adaptive optics in vivo imaging and micro-stimulation,11–13 we created topographical maps of the complete foveolar cone mosaics in both eyes of 20 healthy participants while simultaneously recording the retinal location of a fixated visual object in a psychophysical experiment with cellular resolution. We found that the locus of fixation was systematically shifted away from the topographical center toward a naso-superior quadrant on the retina, about 5 min of arc of visual angle on average, with a mirror symmetrical trend between fellow eyes. In cyclopean view, the topographical centers were superior to the fixated target, corresponding to areas in the visual field usually more distant14,15 and thus containing higher spatial frequencies. Given the large variability in foveal topography between individuals, and the surprising precision with which fixation is repeatedly directed to just a small bouquet of cones in the foveola, these findings demonstrate a finely tuned, functionally relevant link between the development of the cellular mosaic of photoreceptors and visual behavior. [Display omitted] •Foveal cone topography is mirror symmetric between fellow eyes•The preferred retinal locus of fixation (PRL) is reproducible over multiple years•The PRL is offset naso-superiorly on the retina, correlated between fellow eyes•The binocular area of high cone densities is horizontally enlarged, on average Reiniger et al. show that the preferred retinal locus of fixation is systematically and reproducibly displaced from the topographical center of the human fovea. In the binocular visual field, the area of high cone density sampling is thus horizontally enlarged and offset toward an area usually containing smaller details in the natural environment.