The rod signaling pathway in marsupial retinae.

Nicolas D Lutz,Emina Lemes,Silke Haverkamp,Leo Peichl,Leah Krubitzer,Shaun P Collin

doi:10.1371/journal.pone.0202089

Abstract

The retinal rod pathway, featuring dedicated rod bipolar cells (RBCs) and AII amacrine cells, has been intensely studied in placental mammals. Here, we analyzed the rod pathway in a nocturnal marsupial, the South American opossum Monodelphis domestica to elucidate whether marsupials have a similar rod pathway. The retina was dominated by rods with densities of 338,000–413,000/mm². Immunohistochemistry for the RBC-specific marker protein kinase Cα (PKCα) and the AII cell marker calretinin revealed the presence of both cell types with their typical morphology. This is the first demonstration of RBCs in a marsupial and of the integration of RBCs and AII cells in the rod signaling pathway. Electron microscopy showed invaginating synaptic contacts of the PKCα-immunoreactive bipolar cells with rods; light microscopic co-immunolabeling for the synaptic ribbon marker CtBP2 confirmed dominant rod contacts. The RBC axon terminals were mostly located in the innermost stratum S5 of the inner plexiform layer (IPL), but had additional side branches and synaptic varicosities in strata S3 and S4, with S3-S5 belonging to the presumed functional ON sublayer of the IPL, as shown by immunolabeling for the ON bipolar cell marker Gγ13. Triple-immunolabeling for PKCα, calretinin and CtBP2 demonstrated RBC synapses onto AII cells. These features conform to the pattern seen in placental mammals, indicating a basically similar rod pathway in M. domestica. The density range of RBCs was 9,900–16,600/mm2, that of AII cells was 1,500–3,260/mm2. The numerical convergence (density ratio) of 146–156 rods to 4.7–6.0 RBCs to 1 AII cell is within the broad range found among placental mammals. For comparison, we collected data for the Australian nocturnal dunnart Sminthopsis crassicaudata, and found it to be similar to M. domestica, with rod-contacting PKCα-immunoreactive bipolar cells that had axon terminals also stratifying in IPL strata S3-S5.

Highlights

Vision in low light conditions depends on the retinal signaling pathways of the rod photoreceptors
We focus on a nocturnal marsupial, the South American gray short-tailed opossum Monodelphis domestica, which has been introduced as a model species for developmental and comparative research [3]
As rod bipolar cells (RBCs) are depolarized by light stimuli and their axons terminate in the innermost part of the inner plexiform layer (IPL) [14], they are considered to be strictly ON bipolar cells

Summary

Introduction

Vision in low light (scotopic) conditions depends on the retinal signaling pathways of the rod photoreceptors. A hallmark of the retinae of nocturnal placental mammals is the dominance of rod photoreceptors compared to cone photoreceptors [4]. This is true for the nocturnal marsupials that have been investigated [5,6,7,8]. The rod photoreceptors transmit light-induced signals via specialized ribbon synapses from their axon terminals, the rod spherules, to rod bipolar cells (RBCs), which comprise only a single type of bipolar cell compared to about a dozen types of cone bipolar cells [2,13]. We focus on RBCs and the rod signaling pathway of the M. domestica retina and present some comparative data for the Australian nocturnal fat-tailed dunnart Sminthopsis crassicaudata

Methods

Results

Conclusion