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H. Okawa, K. J. Miyagishima, A. P. Sampath; Temporal Filtering of the Single Photon Response in the Mouse Retina. Invest. Ophthalmol. Vis. Sci. 2009;50(13):4567.
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In the dark-adapted mouse retina, the single photon response of rod bipolar cells is faster than the output of rod phototransduction, a transformation that is maintained in ganglion cells. Rod-to-rod bipolar transmission is thus critical for improving the temporal resolution of scotopic vision. Studies from amphibian retina have suggested that this high-pass filtering occurs either in the rod network or in the rod photocurrent-to-photovoltage conversion, but less is known about this process in mammals. To determine the origin of high-pass filtering of the single photon response we compared the rod outer segment photocurrents, rod photovoltages, and rod bipolar photocurrents from wild-type (WT) as well as rhodopsin heterozygous (Rh+/-) and GCAP1/2 knockout (GCAPs-/-) mice, whose rod single photon responses are speeded and slowed compared to WT, respectively.
Suction electrodes from clusters of dissociated retina recorded rod photocurrents. In retinal slices whole-cell patch electrodes recorded rod photovoltages from rod inner segments in current clamp, and rod bipolar currents in voltage clamp (Vm = -60 mV). All tissues were superfused with heated Ames’ media, and full-field 10-ms flashes were delivered from an LED.
The speeded rod photoresponse in Rh+/- mice resulted in an overall speeding of rod bipolar responses. In GCAPs-/- mice the slowed rod photocurrent resulted in rod bipolar photocurrents with a similar time-to-peak as WT, despite the 2.5-fold longer time-to-peak of photocurrent, but overall recovery was slowed. In WT and Rh+/- mice the rod photovoltage already demonstrated the speeding of their rod bipolar counterparts, but in GCAPs-/- mice the time course of the photovoltage was intermediate between the rod photocurrent and the rod bipolar photocurrent. Furthermore, the GCAPs-/- rod bipolar photocurrents were unaffected during internal dialysis with 10 mM BAPTA, indicating that postsynaptic Ca2+ feedback appears not to contribute to the kinetics of their dim flash response.
The kinetics of the rod photocurrent in WT, Rh+/-, and GCAPs-/- mice was reflected generally in the kinetics of the rod bipolar photocurrent. High-pass filtering at the level of the photovoltage can explain the temporal changes in the single photon response for faster responses (WT and Rh+/-). However, for the slower single photon response in GCAPs-/- rods, a presynaptic component downstream of the rod photovoltage is additionally required to explain alterations in the kinetics of the rod bipolar response.
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