Cellular and Circuit Mechanisms Shaping the Perceptual Properties of the Primate Fovea

Abstract

SUMMARY The fovea is a specialized region of the retina that dominates the visual perception of primates by providing high chromatic and spatial acuity. While the foveal and peripheral retina share a similar core circuit architecture, they exhibit profound functional differences whose mechanisms are unknown. Using intracellular recordings and structure-function analyses, we examined the cellular and synaptic underpinnings of the primate fovea. Compared to peripheral vision, the fovea displays decreased sensitivity to rapid variations in light inputs; this difference is reflected in the responses of ganglion cells, the output cells of the retina. Surprisingly, and unlike in the periphery, synaptic inhibition minimally shaped the responses of foveal midget ganglion cells. This difference in inhibition cannot however, explain the differences in the temporal sensitivity of foveal and peripheral midget ganglion cells. Instead, foveal cone photoreceptors themselves exhibit slower light responses than peripheral cones, unexpectedly linking cone signals to perceptual sensitivity.

Development of ON and OFF cholinergic amacrine cells in the human fetal retina

“…The loss of ChAT staining in the OFF layer in the human fovea may be due to a loss of ChAT expression, migration of ChAT cells away from the fovea, or cell death. Although overall, there is very little cell death observed in the fovea after Fwk 20 (Georges, Madigan, & Provis, 1999, Provis & van Driel, 1985, of the fovea (Dacey & Packer, 2003;Provis et al, 2013;Sinha et al, 2017). However, the developmental loss of ChAT-labeled cells in the INL of the fovea is not a universal phenomenon of primate fovea.…”

“…It is perhaps not surprising that there are differences in ChAT cell development between foveal and non‐foveal regions, given the unique structure (avascular), cell arrangement (cone‐rich), circuitry (midget pathway‐dominating), and function (color vision and high spatial acuity) of the fovea (Dacey & Packer, ; Provis et al, ; Sinha et al, ). However, the developmental loss of ChAT‐labeled cells in the INL of the fovea is not a universal phenomenon of primate fovea.…”

Cellular and molecular mechanisms of photoreceptor tuning for prey capture in larval zebrafish

“…For all we know, all sighted vertebrates have at least a mild form of an area temporalis or an area centralis, and in some species such as many primates as well as birds of prey and species of reptiles and fish, these specialised regions have further evolved into a fovea (Bringmann, 2019;Bringmann et al, 2018;Collin et al, 2000;Land, 2015). However, data on the possibility of regional tuning of photoreceptor function across most of these species remains outstanding with the notable exception of primates (Baudin et al, 2019;Sinha et al, 2017), mice (Baden et al, 2013b), and now zebrafish. In each of these latter three, cone-function has been found to be regionally tuned.…”

“…Indeed, photoreceptor tuningeven within-typeis a fundamental property of vision in both invertebrates (Hardie, 1984;Sancer et al, 2019) and vertebrates (Baden et al, 2013b;Baudin et al, 2019;Sinha et al, 2017). Even primates make use of this trick: foveal cones have longer integration times than their peripheral counterparts, likely to boost their signal to noise ratio as in the foveal centre retinal ganglion cells do not spatially pool their inputs (Baudin et al, 2019;Sinha et al, 2017).…”

“…Indeed, photoreceptor tuningeven within-typeis a fundamental property of vision in both invertebrates (Hardie, 1984;Sancer et al, 2019) and vertebrates (Baden et al, 2013b;Baudin et al, 2019;Sinha et al, 2017). Even primates make use of this trick: foveal cones have longer integration times than their peripheral counterparts, likely to boost their signal to noise ratio as in the foveal centre retinal ganglion cells do not spatially pool their inputs (Baudin et al, 2019;Sinha et al, 2017). Understanding the mechanisms that underlie such functional tuning will be important for understanding how sensory systems can operate in the natural sensory world, and how they might have evolved to suit new sensory-ecological niches (Cronin et al, 2014;Lamb et al, 2007;Land and Nilsson, 2012;Yau and Hardie, 2009).…”