Morphological analyses of the retinal photoreceptor cells in the nocturnally adapted owl monkeys

Abstract

Owl monkeys are the only one species possessing the nocturnal lifestyles among the simian monkeys. Their eyes and retinas have been interested associating with the nocturnal adaptation. We examined the cellular specificity and electroretinogram (ERG) reactivity in the retina of the owl monkeys by comparison with the squirrel monkeys, taxonomically close-species and expressing diurnal behavior. Owl monkeys did not have clear structure of the foveal pit by the funduscope, whereas the retinal wholemount specimens indicated a small-condensed spot of the ganglion cells. There were abundant numbers of the rod photoreceptor cells in owl monkeys than those of the squirrel monkeys. However, the owl monkeys' retina did not possess superiority for rod cell-reactivity in the scotopic ERG responses. Scanning electron microscopic observation revealed that the rod cells in owl monkeys' retina had very small-sized inner and outer segments as compared with squirrel monkeys. Owl monkeys showed typical nocturnal traits such as rod-cell dominance. However, the individual photoreceptor cells seemed to be functionally weak for visual capacity, caused from the morphological immaturity at the inner and outer segments.

Keywords: evolution; owl monkey; photoreceptor cell; retina; squirrel monkey.

Fig. 1.

Visual appearances of the owl monkey (A) and the squirrel monkey (B). Note the larger palpebral fissures in owl monkeys than squirrel monkeys. C, D: Eye fundus photographs (left eyes). The optic disc (white arrowheads) is seen in the retina of owl monkey (C) and the squirrel monkey (D), characterized by the extending vascular arches. The central fovea (black arrow) is clearly seen only in the fundus of squirrel monkeys.

Fig. 2.

Retinal topographies of the ganglion cells of owl monkeys (A) and squirrel monkeys (B), measured by the left side of the wholemount specimens. Numbers in the figures represent the density (×10³ cells/mm²). The star figures mean the position of the optic discs. D: distal, V: ventral, N: nasal, T: temporal directions. C–E: Cell densities of cone (C), rod (D) and ganglion cells (E) measured on the wholemount specimens. Ow: owl monkeys; Sq: squirrel monkeys. The lines in each box in graphs mean the 1st, 2nd (median) and 3rd quartile values, respectively. Vertical lines present the range between the maximum and minimum values.

Fig. 3.

Retinal wholemounts. Note the very small photoreceptor cells in the owl monkeys (A) than those of the squirrel monkeys (B). Two types of cells are discriminated as the large cone cells (arrowheads) and the surrounding small rod cells. Inset of A: magnified view of cone and rod cells in the owl monkey. Inset of B: the area of the central fovea in the squirrel monkey. Almost all cells are recognized as cone cells. C, D: Nissl staining of wholemounts can visualize ganglion cells composed by various sizes. Bar scales=20 µm (A, B and inset of B) and 10 µm (C, D and inset of A).

Fig. 4.

SEM photographs of the photoreceptor cells from the retinas of owl monkeys (A, C, D) and squirrel monkeys (B, E, F). Scale bars indicate 100 µm (A, B) and 25 µm (C–F). Arrowheads indicate the inner segments of cone cells (B). C–F: Higher magnification of inner and outer segments of photoreceptor cells. Red lines indicate representative sites for measurements. Asterisks indicate positions of the outer limiting layer. G–I: Results of morphometry for the width of inner segments (IS) of cone (G) and rod cells (H), and combined length of the inner and outer segments (IS+OS) of rod cells (I) in the retinas of owl monkeys (Ow) and squirrel monkeys (Sq). *: P<0.05 and **: P<0.01, vs. squirrel monkeys.

Fig. 5.

Measurements of electroretinogram (ERG) in the owl (Ow) and squirrel (Sq) monkeys. A-F: Representative results for the scotopic (A, D), photopic (B, E), and 30 Hz flicker ERGs (C, F). Arrows and points S indicate the timings of light stimulation. Triangles and characters (a and b) indicate the measurement points. Horizontal axes: time progression (A, D: 25 msec/scale, B, C, E, F: 10 msec/scale). Vertical axis: amplitude (50 µV/scale). Measurements of the latent time (G) and signal amplitudes (H) were compared between both monkeys regarding the scotopic, photopic, and 30 Hz flicker ERGs. *P<0.05.