Retinal ganglion cell topography and spatial resolving power in the river hippopotamus (Hippopotamus amphibius)

Abstract

The river hippopotamus (Hippopotamus amphibius), one of the closest extant relatives to cetaceans, is a large African even-toed ungulate (Artiodactyla) that grazes and has a semiaquatic lifestyle. Given its unusual phenotype, ecology, and evolutionary history, we sought to measure the topographic distribution of retinal ganglion cell density using stereology and retinal wholemounts. We estimated a total of 243,000 ganglion cells of which 3.4% (8,300) comprise alpha cells. The topographic distribution of both total and alpha cells reveal a dual topographic organization of a temporal and nasal area embedded within a well-defined horizontal streak. Using maximum density of total ganglion cells and eye size (35 mm, axial length), we estimated upper limits of spatial resolving power of 8 cycles/deg (temporal area, 1,800 cells/mm ), 7.7 cycles/deg (nasal area, 1,700 cells/mm ), and 4.2 cycles/deg (horizontal streak, 250 cells/mm ). Enhanced resolution of the temporal area toward the frontal visual field may facilitate grazing, while resolution of the horizontal streak and nasal area may help the discrimination of objects (predators, conspecifics) in the lateral and posterior visual fields, respectively. Given the presumed role of alpha cells to detect brisk transient stimuli, their similar distribution to the total ganglion cell population may facilitate the detection of approaching objects in equivalent portions of the visual field. Our finding of a nasal area in the river hippopotamus retina supports the notion that this specialization may enhance visual sampling in the posterior visual field to compensate for limited neck mobility as suggested for rhinoceroses and cetaceans.

Unusual topographic specializations of retinal ganglion cell density and spatial resolution in a cliff‐dwelling artiodactyl, the Nubian ibex (Capra nubiana)

“…Our findings demonstrate that the retina of the Nubian ibex contains typical topographic specializations of high ganglion cell density (i.e., a temporal area, a horizontal streak, and a dorsotemporal extension) found in other artiodactyls examined to date (Coimbra et al, ; Coimbra et al, ; Gonzalez‐Soriano, Mayayo‐Vicente, Martinez‐Sainz, Contreras‐Rodriguez, & Rodriguez‐Veiga, ; Hughes & Whitteridge, ; Shinozaki et al, ). Despite a clear need for detailed topographic studies of the retina of other artiodactyls, the consistent presence of these topographic retinal traits suggests that they may represent an artiodactyl retinal blueprint.…”

“…Our finding of a tapetum lucidum in the Nubian ibex eye is in agreement with the reported activity of this species during dusk and dawn (Groves & Leslie Jr., ). Our data indicate that the occurrence of the tapetum lucidum in the dorsal fundus of the eye of the Nubian ibex is a feature shared with other artiodactyls including the goat, sheep, river hippopotamus, and giraffe (Coimbra et al, ; Coimbra et al, ; Hughes & Whitteridge, ; Shinozaki, Hosaka, Imagawa, & Uehara, ). Similar to the goat and sheep, the tapetum lucidum of the Nubian ibex occupies most of the dorsotemporal portion of the fundus and then tapers toward the nasal retina (Hughes & Whitteridge, ; Shinozaki et al, ).…”

“…Stereological sampling parameters are listed in Table . Retinal ganglion cells were consistently separated from amacrine and glial cells in regions of high and low density using the cytological criteria established by Hughes () and validated in other artiodactyls (Coimbra et al, ; Coimbra et al, ) (Figure d,e).…”

“…Similar to the goat and sheep, the tapetum lucidum of the Nubian ibex occupies most of the dorsotemporal portion of the fundus and then tapers toward the nasal retina (Hughes & Whitteridge, ; Shinozaki et al, ). This spatial distribution contrasts with the broad coverage of tapetum across the dorsal fundus in the giraffe and river hippopotamus (Coimbra et al, ; Coimbra et al, ). The reasons for these differences are unclear, but they may reflect specific ecological needs for enhanced visual sensitivity across these species.…”

“…Eye size and maximum density of retinal ganglion cells are two important factors that influence the spatial resolving power of the eye (Pettigrew et al, ; Veilleux & Kirk, ). In artiodactyls examined to date, anatomical estimates of spatial resolving power based on retinal ganglion cell peak density and eye axial length range between ~8 cycles/degree (river hippopotamus) and 27 cycles/degree (giraffe) (Coimbra et al, ; Coimbra et al, ; Hughes & Whitteridge, ; Shinozaki et al, ). Specifically, our estimate of spatial resolving power of ~17 cycles/degree in the Nubian ibex is within the range of the spatial resolving power estimated for other closely related Caprinae (Goat, ~13 cycles/degree; Sheep, ~22 cycles/degree).…”