A fibrous membrane suspends the multifocal lens in the eyes of lampreys and African lungfishes

Abstract

The sharpness and thus information content of the retinal image in the eye depends on the optical quality of the lens and its accurate positioning in the eye. Multifocal lenses create well-focused color images and are present in the eyes of all vertebrate groups studied to date (mammals, reptiles including birds, amphibians, and ray-finned fishes) and occur even in lampreys, i.e., the most basal vertebrates with well-developed eyes. Results from photoretinoscopy obtained in this study indicate that the Dipnoi (lungfishes), i.e., the closest piscine relatives to tetrapods, also possess multifocal lenses. Suspension of the lens is complex and sophisticated in teleosts (bony fishes) and tetrapods. We studied lens suspension using light and electron microscopy in one species of lamprey (Lampetra fluviatilis) and two species of African lungfish (Protopterus aethiopicus aethiopicus and Protopterus annectens annectens). A fibrous and highly transparent membrane suspends the lens in both of these phylogenetically widely separated vertebrate groups. The membrane attaches to the lens approximately along the lens equator, from where it extends to the ora retinalis. The material forming the membrane is similar in ultrastructure to microfibrils in the zonule fibers of tetrapods. The membrane, possibly in conjunction with the cornea, iris, and vitreous body, seems suitable for keeping the lens in the correct position for well-focused imaging. Suspension of the lens by a multitude of zonule fibers in tetrapods may have evolved from a suspensory membrane similar to that in extant African lungfishes, a structure that seems to have appeared first in the lamprey-like ancestors of allextant vertebrates.

Optical advantages and function of multifocal spherical fish lenses

“…The evolutionary adaptation of visual pigments occurs by genetic changes, either in the expression of pigment genes [46] or mutations in the opsin genes leading to amino acid substitutions in the opsin molecule [47][48][49][50][51]. Here we have shown that the optical properties of the lens should match the spectral composition of the retina in order to maximize optical performance, indicating that there should be an equally large variation in the optical properties of fish lenses, and this has indeed been observed [10,11,[37][38][39][40]. Interestingly, changes in the optical properties of fish lenses can be induced by environmental parameters and take place within a few hours to months [13,52].…”

“…A natural fish lens with a smooth LSA curve may transfer more information than the step-function lens with well-defined refractive zones with sharp transitions between focal lengths. In fish there is a large variety of multifocal lenses, including ones with several refractive zones focusing similar spectral ranges [10,11,[37][38][39][40]. Analysis of these phenomena and adaptations was beyond the scope of our work.…”

“…In animals with color vision and eyes of small f -numbers, i.e., short depth of focus, this tradeoff between spatial and spectral information seems to be more favorable with multifocal lenses. Many vertebrate species, both aquatic and terrestrial, have such lenses [10,11,[14][15][16][37][38][39][40][41].…”

The Retinal Wholemount Technique: A Window to Understanding the Brain and Behaviour

“…These include the following: (1) the position and shape of the optic nerve head, including multiple Sharma, 1987, 1988] and elongated [Collin et al, 2000] optic nerve heads; (2) any remaining scars due to the healing (or partial healing) of the embryonic fissure or falciform process [Collin and Pettigrew, 1988a]; (3) the shape and depth of any foveal pit or depression in the retina [Collin and Collin, 1999;Collin et al, 2000;Moroney and Pettigrew, 1987;Wood, 1917]; (4) retinal thickening(s) across the retinal meridian typically indicating the position of one or more horizontal/visual streaks [Munk, 1970]); (5) differences in the size, shape and attachment of the lens [Gustafsson et al, 2010;Khorramshahi et al, 2008]; (6) the presence or absence of vitreal vascularization, a conus or a pecten [Collin, 1989a;Hanyu, 1962;Nguyen, 1970;Smith et al, 1996;Yu et al, 2009], and (7) colored eye shine produced by any tapetal material underlying the retina to increase visual sensitivity [Braekevelt, 1986[Braekevelt, , 1990Collin and Collin, 1993;Nicol, 1981]. The presence of these morphological and, in many cases, species-or taxon-specific variables presents technical difficulties.…”

Vision in elasmobranchs and their relatives: 21st century advances

“…The lens is held in position by a combination of a suspensory ligament in association with an intraocular muscle. Given the recent finding that the lens suspension mechanisms in bony fishes are more complex than was classically thought (Khorramshahi et al , 2008; Gustafsson et al , 2010), it would be interesting to reinvestigate lens suspension in cartilaginous fishes.…”