Delayed neurogenesis with respect to eye growth shapes the pigeon retina for high visual acuity

Abstract

The macula and fovea located at the optical centre of the retina make primate visual perception unique among mammals. Our current understanding of retina ontogenesis is primarily based on animal models having no macula and no fovea. However, the pigeon retina and the human macula share a number of structural and functional properties that justify introducing the former as a new model system for retina development. Comparative transcriptome analysis of pigeon and chicken retinas at different embryonic stages reveals that the genetic programmes underlying cell differentiation are postponed in the pigeon until the end of the period of cell proliferation. We show that the late onset of neurogenesis has a profound effect on the developmental patterning of the pigeon retina, which is at odds with the current models of retina development. The uncoupling of tissue growth and neurogenesis is shown to result from the fact that the pigeon retinal epithelium is inhibitory to cell differentiation. The sum of these developmental features allows the pigeon to build a retina that displays the structural and functional traits typical of primate macula and fovea.

Fgf8 Expression and Degradation of Retinoic Acid Are Required for Patterning a High-Acuity Area in the Retina

“…In keeping with this notion, the broad equatorial RA-free streak in mice coincides with a moderately increased density of RGCs in this region. Investigation of the Cyp26s spot and stripe patterns in bi-foveated bird species, with a central and a temporal HAA, e.g., birds of prey (Slonaker, 1897; Fite and Rosenfield-Wessels, 1975), and pigeons who possess a second HAA in the dorsal area (Querubin et al, 2009; Rodrigues et al, 2016), will also prove interesting insights regarding the function of such patterns.…”

The Appearance of the Warburg Effect in the Developing Avian Eye Characterized In Ovo: How Neurogenesis Can Remodel Neuroenergetics

“…Bird eggs were hatched in a portable incubator keeping humidity and temperature (37°C) of the ambient air at optimal conditions for embryo development. 12 A group of six animals were scanned longitudinally in the MRS experiments, and all other experiments were performed on individual groups described in each section. Because of the technical constraints of 1 H-MRS, focus was put on the embryonic stages E6 and E8 for the in vivo measurements to reflect the peak in RGC production in the chick occurring at day 6.…”

“…Because of the technical constraints of 1 H-MRS, focus was put on the embryonic stages E6 and E8 for the in vivo measurements to reflect the peak in RGC production in the chick occurring at day 6. 12 A detailed description of the Materials and Methods used can be found in the Supplementary Material. Statistical analyses are explained in the Supplementary Material and in the figure legends.…”

“…11 With a focus on the avian eye, we take these studies a step further to characterize how energy metabolism (i.e., glycolytic and oxidative intermediates and/or products) is associated with structure and compartmentation during the time window of retinal neurogenesis using in vivo 1 H-magnetic resonance spectroscopy ( 1 H-MRS) at ultra-high magnetic field. We capitalized on the fact that both chick and pigeon retinas grow at a similar pace; yet, cell differentiation and the production of RGCs are delayed by approximately 3 days in the pigeon, 12 providing a strategy to directly link our MRS measurements to metabolic adaptations taking place during neurogenesis.…”

Single cell transcriptome profiling of developing chick retinal cells

“…Multiple studies examining RGC birth have yielded a window for RGC birthdates that spans from embryonic day 3 (E3) through E8 (Mey & Thanos, ; Sakagami et al, ; Snow & Robson, ; Spence & Robson, ) with full RGC differentiation not completed until E16 (Mey & Thanos, ). The majority of these cells are born before the plexiform layers begin to form, as the GCL and inner plexiform layer (IPL) cannot be observed until E7, and the outer plexiform layer (OPL) does not begin to develop until E9 (Rodrigues et al, ; Spence & Robson, ). This first birth wave also sees production of ACs from E3 to E14, depending upon their subtype and location in the retina (Mey & Thanos, ; Snow & Robson, ; Spence & Robson, ).…”