Retinal Amino Acid Neurochemistry of the Southern Hemisphere Lamprey, Geotria australis

Abstract

Lampreys are one of the two surviving groups of the agnathan (jawless) stages in vertebrate evolution and are thus ideal candidates for elucidating the evolution of visual systems. This study investigated the retinal amino acid neurochemistry of the southern hemisphere lamprey Geotria australis during the downstream migration of the young, recently-metamorphosed juveniles to the sea and during the upstream migration of the fully-grown and sexually-maturing adults to their spawning areas. Glutamate and taurine were distributed throughout the retina, whilst GABA and glycine were confined to neurons of the inner retina matching patterns seen in most other vertebrates. Glutamine and aspartate immunoreactivity was closely matched to Müller cell morphology. Between the migratory phases, few differences were observed in the distribution of major neurotransmitters i.e. glutamate, GABA and glycine, but changes in amino acids associated with retinal metabolism i.e. glutamine and aspartate, were evident. Taurine immunoreactivity was mostly conserved between migrant stages, consistent with its role in primary cell functions such as osmoregulation. Further investigation of glutamate signalling using the probe agmatine (AGB) to map cation channel permeability revealed entry of AGB into photoreceptors and horizontal cells followed by accumulation in inner retinal neurons. Similarities in AGB profiles between upstream and downstream migrant of G. australis confirmed the conservation of glutamate neurotransmission. Finally, calcium binding proteins, calbindin and calretinin were localized to the inner retina whilst recoverin was localized to photoreceptors. Overall, conservation of major amino acid neurotransmitters and calcium-associated proteins in the lamprey retina confirms these elements as essential features of the vertebrate visual system. On the other hand, metabolic elements of the retina such as neurotransmitter precursor amino acids and Müller cells are more sensitive to environmental changes associated with migration.

Characterization and Evolution of the Spotted Gar Retina

“…Across all species displayed, differences in location of HCs have been observed, and large varieties of photoreceptor types are predicted and/or observed (Figs. B–D and I–M) (Ali and Anctil, ; Dartnall et al., ; Boynton, ; Applebury et al., ; Collin et al., ; Connaughton et al., ; Roberts et al., ; Takechi and Kawamura, ; Song et al., ; Allison et al., ; Lagman et al., ; Nivison‐Smith et al., ). Much remains unknown, but being able to directly compare specialized tissue, such as the retina, across species that have long diverged in evolution provides an opportunity to understand how biological systems develop.…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…The adult retina contains all types of retinal cells found in gnathostomes: photoreceptors (rods and cones), bipolar cells, horizontal cells, amacrine cells and different types of retinal ganglion cells (RGCs) (Figs and C) as well as interplexiform neurons (Villar‐Cerviño et al, ). The retina of downstream‐migrating transformers is densely packed with cells, while the older upstream migrants have a larger retina with sparsely distributed, larger cells (Nivison‐Smith et al, ). No proliferating cells were found by Villar‐Cheda et al () in the adult retina, which suggests that the increase in retinal surface area and volume in the adult stage is mainly due to growth in cell size and cellular reorganisation.…”

Tryptophan hydroxylase and serotonin receptor 1A expression in the retina of the sea lamprey

“…Long and short photoreceptors of the adult sea lamprey are difficult to assign to rod or cones (see Collin et al, 2009), but express rod-like and cone type transducins, respectively (Muradov et al, 2008). In the southern hemisphere lamprey, Geotria australis, five types of retinal photoreceptor express five types of cone opsins and its retina shows higher complexity than those of northern hemisphere lampreys (Davies et al, 2007;Collin et al, 2009;Nivison-Smith et al, 2013).…”