Ancient origin of the rod bipolar cell pathway in the vertebrate retina

Hellevik, Ayana M.; Mardoum, Philip; Hahn, Joshua; Kölsch, Yvonne; D’Orazi, Florence D.; Suzuki, Sachihiro C.; Godinho, Leanne; Lawrence, Owen; Rieke, Fred; Shekhar, Karthik; Sanes, Joshua R.; Baier, Herwig; Baden, Tom; Wong, Rachel O.; Yoshimatsu, Takeshi

doi:10.1038/s41559-024-02404-w

Nat Ecol Evol

2024

DOI: 10.1038/s41559-024-02404-w

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Ancient origin of the rod bipolar cell pathway in the vertebrate retina

Ayana M. Hellevik,

Philip Mardoum,

Joshua Hahn

et al.

Abstract: Highlights-Zebrafish have two rod bipolar cell types (RBC1/2).-Synaptic connectivity of RBC1 resembles that of the mammalian RBCs.-The primary rod pathway therefore probably evolved more than 400 million years ago.-The second zebrafish RBC type, RBC2, forms a separate pathway from RBC1.

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Nanophysiology Approach Reveals Diversity in Calcium Microdomains in Zebrafish Retinal Bipolar Ribbon Synapses

Rameshkumar,

Shrestha,

Boff

et al. 2024

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Rapid and high local calcium (Ca2+) signals are essential for triggering neurotransmitter release from presynaptic terminals. In specialized bipolar ribbon synapses in the retina, these local Ca2+ signals control multiple processes, including the priming, docking, and translocation of vesicles on the ribbon before exocytosis and the replenishment of release-ready vesicles to the fusion sites to sustain neurotransmission. However, our knowledge about Ca2+ signals along the axis of the ribbon active zone is limited. Here, we used fast confocal quantitative dual-color ratiometric line-scan imaging of a fluorescently labeled ribbon binding peptide and Ca2+ indicators to monitor the spatial and temporal aspects of Ca2+ transients of individual ribbon active zones in zebrafish retinal rod bipolar cells. We observed that a Ca2+ transient elicited a much greater fluorescence amplitude when the Ca2+ indicator was conjugated to a ribeye-binding peptide than when using a soluble Ca2+ indicator, and the estimated Ca2+ levels at the ribbon active zone exceeded 26 μM in response to a 10-millisecond stimulus, as measured by a ribbon-bound low-affinity Ca2+ indicator. Our quantitative modeling of Ca2+ diffusion and buffering is consistent with this estimate and provides a detailed view of the spatiotemporal [Ca2+] dynamics near the ribbon. Importantly, our data demonstrates that the local Ca2+ levels may vary between ribbons of different rod bipolar cells and within the same cells. The variation in local Ca2+ signals is likely due to heterogeneity in local Ca2+ channels clustered at the ribbon active zone, as serial electron microscopy provides new information about the heterogeneity in ribbon size, shape, and area of the ribbon in contact with the plasma membrane.

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Nanophysiology Approach Reveals Diversity in Calcium Microdomains in Zebrafish Retinal Bipolar Ribbon Synapses

Rameshkumar,

Shrestha,

Boff

et al. 2024

Preprint

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Ancient origin of the rod bipolar cell pathway in the vertebrate retina

Abstract: Highlights-Zebrafish have two rod bipolar cell types (RBC1/2).-Synaptic connectivity of RBC1 resembles that of the mammalian RBCs.-The primary rod pathway therefore probably evolved more than 400 million years ago.-The second zebrafish RBC type, RBC2, forms a separate pathway from RBC1.

Cited by 1 publication

References 107 publications

Nanophysiology Approach Reveals Diversity in Calcium Microdomains in Zebrafish Retinal Bipolar Ribbon Synapses

Nanophysiology Approach Reveals Diversity in Calcium Microdomains in Zebrafish Retinal Bipolar Ribbon Synapses

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