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The Journal of Neuroscience, July 5, 2006, 26(27):7201-7211; doi:10.1523/JNEUROSCI.5230-05.2006

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Cellular/Molecular
Scotopic Visual Signaling in the Mouse Retina Is Modulated by High-Affinity Plasma Membrane Calcium Extrusion

Jacque L. Duncan,¹ Haidong Yang,¹ Thuy Doan,² Robert S. Silverstein,⁴ Gabe J. Murphy,^3,4 George Nune,¹ Xiaorong Liu,¹ David Copenhagen,^1,2 Bruce L. Tempel,⁴ Fred Rieke,^3,4 and David Kriaj¹

Departments of ¹Ophthalmology and ²Physiology, University of California San Francisco School of Medicine, San Francisco, California 94143-0730, ³Departments of Physiology and Biophysics and Howard Hughes Medical Institute, and ⁴Otolaryngology–Head and Neck Surgery and the Neurobiology and Behavior Program, University of Washington School of Medicine, Seattle, Washington 98195

Correspondence should be addressed to David Kriaj, Department of Ophthalmology, Beckman Vision Center, Room K-131, University of California, San Francisco School of Medicine, 10 Koret Way, San Francisco, CA 94143-0730. Email: krizaj{at}phy.ucsf.edu

Transmission of visual signals at the first retinal synapse is associated with changes in calcium concentration in photoreceptors and bipolar cells. We investigated how loss of plasma membrane Ca²⁺ ATPase isoform 2 (PMCA2), the calcium transporter isoform with the highest affinity for Ca²⁺/calmodulin, affects transmission of rod- and cone-mediated responses. PMCA2 expression in the neuroblast layer was observed soon after birth; in the adult, PMCA2 was expressed in inner segments and synaptic terminals of rod photoreceptors, in rod bipolar cells, and in most inner retinal neurons but was absent from cones. To determine the role of PMCA2 in retinal signaling, we compared morphology and light responses of retinas from control mice and deafwaddler dfw^2J mice, which lack functional PMCA2 protein. The cytoarchitecture of retinas from control and dfw^2J mice was indistinguishable at the light microscope level. Suction electrode recordings revealed no difference in the sensitivity or amplitude of outer segment light responses of control and dfw^2J rods. However, rod-mediated ERG b-wave responses in dfw^2J mice were 45% smaller and significantly slower than those of control mice. Furthermore, recordings from individual rod bipolar cells showed that the sensitivity of transmission at the rod output synapse was reduced by 50%. No changes in the amplitude or timing of cone-mediated ERG responses were observed. These results suggest that PMCA2-mediated Ca²⁺ extrusion modulates the amplitude and timing of the high-sensitivity rod pathway to a much greater extent than that of the cone pathway.

Key words: photoreceptor; PMCA; deafwaddler; retina; ERG; slice

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Received July 10, 2004; revised April 28, 2006; accepted April 30, 2006.

Correspondence should be addressed to David Kriaj, Department of Ophthalmology, Beckman Vision Center, Room K-131, University of California, San Francisco School of Medicine, 10 Koret Way, San Francisco, CA 94143-0730. Email: krizaj{at}phy.ucsf.edu

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