Intraretinal variability and specialization of cones in Japanese anchovy (Engraulis japonicus, Engraulidae)

Abstract

The retina of anchovies is characterized by an unusual arrangement and ultrastructure of cones. In the retina of Japanese anchovies, Engraulis japonicus, three types of cones are distributed into rows. The nasal, central, temporal, and ventro-temporal regions of the retina were occupied exclusively by the long and short cones. Triple cones, made up of two lateral components and one smaller central component, were found only in the dorsal and ventro-nasal retinal regions. In the outer segments of all short and long cones from the ventro-temporal region, the lamellae were oriented along the cell axis and were perpendicular to the lamellae in the long cones, providing a morphological basis for the detection of polarization. This lamellar orientation is unique to all vertebrates. The cones were examined with respect to regional differentiation in their size and spectral properties via light microscopy, transmission electron microscopy, and microspectrophotometry. Various dimensions of cones were measured in preparations of isolated cells. The cones from the ventro-temporal region had different dimensions than cones of the same type located in other retinal regions. Triple cones from the dorsal region were significantly larger than triple cones from the ventro-nasal region. The spectral absorbance of the lateral components of triple cones in the ventro-nasal retina was identical to the absorbance of all long and short cones from the ventro-temporal region. These are shifted to shorter wavelengths relative to the absorbance of the lateral components of the triple cones located in the dorsal retina. Thus, the retina of the Japanese anchovy shows some features of regional specialization common in other fishes that improves spatial resolution for the upwards and forwards visual axis and provides spectral tuning in downwelling light environment. That results from the differentiation of cone types by size and by different spectral sensitivity of various retinal areas.

Variation in opsin transcript expression explains intraretinal differences in spectral sensitivity of the northern anchovy

“…The short wavelength sensitivity could be mediated by the lateral cones of triple cone units, which house an M visual pigment (Novales Flamarique, 2017). It is noteworthy that the outer segment of the central cone is much smaller than that of the lateral cone (Heß, 2009; Novales Flamarique, 2011; Kondrashev et al, 2016), and this may explain, through a negative interaction between cone types, the diminished sensitivity at longer wavelengths (e.g., 560 nm) compared to that at shorter wavelengths (e.g., 500 nm). It is also possible that a short wavelength visual pigment may be present in anchovies (contributing, for instance, to the increased sensitivity at 480 nm in the DN retina, Fig.…”

“…Retinal sectors: DT, dorso-temporal; DN, dorso-nasal; VN, ventro-nasal; and VT, ventro-temporal an M visual pigment (Novales Flamarique, 2017). It is noteworthy that the outer segment of the central cone is much smaller than that of the lateral cone (Heß, 2009; Novales Flamarique, 2011; Kondrashev et al, 2016), and this may explain, through a negative interaction between cone types, the diminished sensitivity at longer wavelengths (e.g., 560 nm) compared to that at shorter Fig. 3.…”

A vertebrate retina with segregated colour and polarization sensitivity

“…Although the microvillar arrangement between retinular cells can vary from stacked to non-overlapping, most invertebrates with both colour and polarization vision that have been studied have a segregated retina that independently detects and processes these two attributes of light [1,[7][8][9]. Among vertebrates, with the exception of some humans [11], whose polarization sensitivity manifests itself as Haidinger's brushes to no practical significance, the only species with a demonstrated photoreceptor basis explaining their polarization sensitivity are anchovies in the family Engraulididae [12][13][14][15][16][17][18][19][20][21]. Reports of polarization sensitivity in other vertebrates are controversial [22][23][24][25] and the photoreceptor detection models to explain such sensitivity are speculative [26].…”

“…It is only in anchovies where a detection model based on axial dichroism of cone photoreceptors has been confirmed using side-on measurements of polarized light absorbance showing maximal absorption for polarization along the outer segment's length [21]. Unlike the cone photoreceptors in other vertebrates, where the visual pigment-laden outer segment lamellae are oriented transversely to the photoreceptor's axis, those of some anchovies are oriented parallel to the photoreceptor's length [12,[14][15][16][17][18][19][20][21]. Such a structural specialization makes these photoreceptors sensitive to the polarization of incident light as the visual pigment chromophores are confined to the plane of the lamellae [21].…”

“…During the last decade, studies of anchovy photoreceptors have revealed an assortment of unique cone types that define various retinal domains [13,15,16,18]. Cones with longitudinally oriented lamellae are found only in the ventro-temporal (VT) retina, and consist of rows of alternating long and short cones (the latter with bilobed outer segments) that have lamellae perpendicular to each other and to the incident illumination [15,16,18]. These cones form an orthogonal set of polarizationsensitive photoreceptors [21] and, in the northern anchovy, Engraulis mordax, mediate polarization sensitivity at the level of the optic nerve [20].…”