Retinal amino acid neurochemistry of the southern hemisphere lamprey, Geotria australis.

Lisa Nivison-Smith,Michael Kalloniatis,Ian C Potter,Yuan Zhu,Shaun P Collin,David M Hunt,Sarah Ready,Monica L Acosta

doi:10.1371/journal.pone.0058406

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.

Highlights

IntroductionTogether with the hagfishes, are the sole survivors of the early agnathan (jawless) stages in vertebrate evolution [1,2]
Lampreys, together with the hagfishes, are the sole survivors of the early agnathan stages in vertebrate evolution [1,2]
The ganglion cells in the lamprey retina are mostly displaced to the inner nuclear layer (INL) near the inner plexiform layer (IPL) border with few ganglion cells situated in the middle of the IPL and adjoining the inner limiting membrane (Figure 1; [12,13])

Summary

Introduction

Together with the hagfishes, are the sole survivors of the early agnathan (jawless) stages in vertebrate evolution [1,2]. The lamprey retina conforms to the common structure and composition observed in most vertebrate eyes [8]. Neurons are organised into discrete layers of cell bodies and axonal and dendritic processes; i.e. nuclear and plexiform layers. Photoreceptors are located sclerad to second and third order neurons, including bipolar, horizontal, amacrine and ganglion cells situated closer to the vitreous [9,10,11]. The ganglion cells in the lamprey retina are mostly displaced to the inner nuclear layer (INL) near the inner plexiform layer (IPL) border with few ganglion cells situated in the middle of the IPL and adjoining the inner limiting membrane (Figure 1; [12,13])

Methods

Results

Discussion

Conclusion