Foveate vision in deep–sea teleosts: a comparison of primary visual and olfactory inputs

Abstract

The relative importance of vision in a foveate group of alepocephalid teleosts is examined in the context of a deep-sea habitat beyond the penetration limits of sunlight. ) and retinal ganglion cell (11.9 £ 10 3 cells mm 7 2 ) densities peak within the foveal clivus and the perifoveal slopes, respectively, with a centro-peripheral gradient between 3:1 (photoreceptors) and over 20:1 (ganglion cells). The marked increase in retinal sampling localized in temporal retina, coupled with a high summation ratio (13:1), suggest that foveal vision optimizes both spatial resolving power and sensitivity in the binocular frontal visual ¢eld. The elongated optic nerve head is comprised of over 500 optic papillae, which join at the embryonic ¢ssure to form a thin nervous sheet behind the eye. The optic nerve is divided into two axonal bundles; one receiving input from the fovea (only unmyelinated axons) and the other from non-specialized retinal regions (25% of axons are myelinated), both of which appear to be separated as they reach the visual centres of the central nervous system. Comparison of the number of primary (¢rst-order) axonal pathways for the visual (a total of 63.4 £10 6 rod photoreceptors) and olfactory (a total of 15. ), vision appears to play a major role in the survival of these deep-sea teleosts and emphasizes that ecological and behavioural strategies account for signi¢cant variation in sensory brain structure.

Allometric Scaling of the Optic Tectum in Cartilaginous Fishes

“…The smallest tecta were found in all benthic sharks and batoids and the majority of bathyal species. The patterns of midbrain organization we report here reflect those found in bony fishes, especially teleosts [reviewed in Kotrschal et al, 1998; also see Collin et al, 2000 andWagner, 2001a, b]. Similar studies have linked variation in the relative size of the optic tectum in amphibians [Roth et al, 1992] and birds [Cobb, 1964;Boire and Baron, 1994;Iwaniuk and Hurd, 2005;Striedter, 2005] and the superior colliculus (analogous to the optic tectum) in mammals [Tilney, 1927;Langworthy, 1967;Baron et al, 1996;Oelschlager et al, 2008].…”

“…We present what we believe to be the first documented attempt to uncover a correction factor for optic tectum volume measured using the idealized half-ellipsoid approach (method E) compared to tectum volume established using coronal sections (method S) in cartilaginous fishes. Although it is a lesssophisticated technique in comparison to other forms of neuro-morphological analysis [Wagner, 2001a;Ullmann et al, 2010], the half-ellipsoid and ellipsoid methods are expeditious, non-invasive, and have been widely used in recent years to assess sensory specializations and the relative importance of various senses in a range of fishes, such as cichlids [Huber et al, 1997;Pollen et al, 2007], deep-sea fishes [Collin et al, 2000;Wagner, 2001aWagner, , b, 2002Wagner, , 2003], large sharks and teleosts , and elasmobranchs . These techniques have proved particularly useful for making inferences about the sensory ecology and behavior of little-known or largely inaccessible species, which is especially pertinent given that many cartilaginous fishes are relatively large marine animals, are often highly migratory and/or live in deepwater, are potentially dangerous, and are very difficult to keep in captivity [Gruber and Myrberg, 1977;Nelson, 1977].…”

“…Optic tectum size is correlated with eye size, retinal area, the number of retinal ganglion cells, and the number of axons in the optic nerve [Huber and Rylander, 1992;Collin et al, 2000]. Enlarged optic tecta are associated with various ecological niche factors in teleost fishes, such as a diurnal lifestyle, inhabiting clear water (shallow or deep), and piscivory, or feeding on other mobile prey [reviewed in Kotrschal et al, 1998; see also Wagner, 2001a, b;Ito et al, 2007].…”

Retinal Ganglion Cell Distribution and Spatial Resolving Power in Deep-Sea Lanternfishes (Myctophidae)

“…Areae have been found in several tubular and non-tubular eyed deep-sea species of teleosts, providing acute vision in different parts of the visual field depending on the location of the specialization [Collin and Partridge, 1996;Wagner et al, 1998]. A fovea, a pit-like invagination of the retina associated with an area, has also been observed in several species [Collin and Partridge, 1996;Wagner et al, 1998;Collin et al, 2000], providing high acuity and possibly image magnification, accurate fixation and depth perception [Walls, 1942]. Finally, relatively unspecialiszed retinas with a nearly uniform ganglion cell distribution, probably mediating high sensitivity rather than acuity, have also been reported in a single group of deep-sea fishes, the Myctophidae [Wagner et al, 1998].…”

The Organization of the Inner Retina in a Pure-Rod Deep-Sea Fish

“…Questions of retinal processing have been approached mainly in statistical terms and demonstrated high convergence ratios from the rods via presumed bipolar to ganglion cells, often similar to cat retinae [Wagner et al, 1998]. In addition, the topography of ganglion cells has been studied, and striking pattens of specializations including areae and foveae have been revealed especially for mesopelagic species [Collin and Partridge, 1996;Collin et al, 2000].…”